دورية أكاديمية

The genetic and ecophysiological diversity of Microcystis.

التفاصيل البيبلوغرافية
العنوان: The genetic and ecophysiological diversity of Microcystis.
المؤلفون: Dick GJ; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA.; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA., Duhaime MB; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA., Evans JT; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA., Errera RM; National Oceanographic and Atmospheric Administration Great Lakes Environmental Research Lab, Ann Arbor, MI, USA., Godwin CM; School for Environment and Sustainability, Cooperative Institute for Great Lakes Research, University of Michigan, Ann Arbor, MI, USA., Kharbush JJ; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA., Nitschky HS; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA., Powers MA; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA., Vanderploeg HA; National Oceanographic and Atmospheric Administration Great Lakes Environmental Research Lab, Ann Arbor, MI, USA., Schmidt KC; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA., Smith DJ; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA., Yancey CE; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA., Zwiers CC; Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA., Denef VJ; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA.
المصدر: Environmental microbiology [Environ Microbiol] 2021 Dec; Vol. 23 (12), pp. 7278-7313. Date of Electronic Publication: 2021 Jun 14.
نوع المنشور: Journal Article; Research Support, U.S. Gov't, Non-P.H.S.; Review
اللغة: English
بيانات الدورية: Publisher: Blackwell Science Country of Publication: England NLM ID: 100883692 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1462-2920 (Electronic) Linking ISSN: 14622912 NLM ISO Abbreviation: Environ Microbiol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Oxford : Blackwell Science, 1999-
مواضيع طبية MeSH: Cyanobacteria* , Microcystis*/genetics, Ecosystem
مستخلص: Microcystis is a cyanobacterium that forms toxic blooms in freshwater ecosystems around the world. Biological variation among taxa within the genus is apparent through genetic and phenotypic differences between strains and via the spatial and temporal distribution of strains in the environment, and this fine-scale diversity exerts strong influence over bloom toxicity. Yet we do not know how varying traits of Microcystis strains govern their environmental distribution, the tradeoffs and links between these traits, or how they are encoded at the genomic level. Here we synthesize current knowledge on the importance of diversity within Microcystis and on the genes and traits that likely underpin ecological differentiation of taxa. We briefly review spatial and environmental patterns of Microcystis diversity in the field and genetic evidence for cohesive groups within Microcystis. We then compile data on strain-level diversity regarding growth responses to environmental conditions and explore evidence for variation of community interactions across Microcystis strains. Potential links and tradeoffs between traits are identified and discussed. The resulting picture, while incomplete, highlights key knowledge gaps that need to be filled to enable new models for predicting strain-level dynamics, which influence the development, toxicity and cosmopolitan nature of Microcystis blooms.
(© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.)
References: Agha, R., del Mar Labrador, M., de los Ríos, A., and Quesada, A. (2016) Selectivity and detrimental effects of epiphytic Pseudanabaena on Microcystis colonies. Hydrobiologia 777: 139-148.
Agrawal, A.A. (2001) Phenotypic plasticity in the interactions and evolution of species. Ecology 294: 321-326.
Agrawal, A.A., and Van Zandt, P.A. (2003) Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed. J Ecol 91: 1049-1059.
Ahlgren, G. (1985) Growth of Oscillatoria agardhii in chemostat culture 3. Simultaneous limitation of nitrogen and phosphorus. Br Phycol J 20: 249-261.
Akins, L., Ortiz, J., and Leff, L.G. (2020) Strain-specific responses of toxic and non-toxic Microcystis aeruginosa to exudates of heterotrophic bacteria. Hydrobiologia 847: 75-89.
Alexova, R., Dang, T.C., Fujii, M., Raftery, M.J., Waite, T.D., Ferrari, B.C., and Neilan, B.A. (2016) Specific global responses to N and Fe nutrition in toxic and non-toxic Microcystis aeruginosa. Environ Microbiol 18: 401-413.
Alexova, R., Haynes, P.A., Ferrari, B.C., and Neilan, B.A. (2011) Comparative protein expression in different strains of the bloom-forming cyanobacterium Microcystis aeruginosa. Mol Cell Proteomics 10: M110.003749.
Amé, M.V., and Wunderlin, D.A. (2005) Effects of iron, ammonium and temperature on microcystin content by a natural concentrated Microcystis aeruginosa population. Water Air Soil Pollut 168: 235-248.
Amin, S.A., Hmelo, L.R., Van Tol, H.M., Durham, B.P., Carlson, L.T., Heal, K.R., et al. (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522: 98-101.
Andeer, P.F., Learman, D.R., Mcilvin, M., Dunn, J.A., and Hansel, C.M. (2015) Extracellular haem peroxidases mediate Mn ( II ) oxidation in a marine Roseobacter bacterium via superoxide production. 17: 3925-3936.
Anderson, C.R., Johnson, H.A., Caputo, N., Davis, R.E., Torpey, J.W., and Tebo, B.M. (2009) Mn(II) oxidation is catalyzed by heme peroxidases in “Aurantimonas manganoxydans” strain SI85-9A1 and Erythrobacter sp. strain SD-21. Appl Environ Microbiol 75: 4130-4138.
Arandia-Gorostidi, N., Weber, P.K., Alonso-Sáez, L., Morán, X.A.G., and Mayali, X. (2017) Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment. ISME J 11: 641-650.
Arevalo, P., VanInsberghe, D., and Polz, M.F. (2018) A reverse ecology framework for Bacteria and Archaea. In Population Genomics: Microorganisms. Cham, Switzerland: Springer, pp. 77-96.
Baker, J.A., Entsch, B., Neilan, B.A., and McKay, D.B. (2002) Monitoring changing toxigenicity of a cyanobacterial bloom by molecular methods. Appl Environ Microbiol 68: 6070-6076.
Baldia, S.F., Evangelista, A.D., Aralar, E.V., and Santiago, A.E. (2007) Nitrogen and phosphorus utilization in the cyanobacterium Microcystis aeruginosa isolated from Laguna de bay, Philippines. J Appl Phycol 19: 607-613.
Bañares-España, E., López-Rodas, V., Salgado, C., Costas, E., and Flores-Moya, A. (2006) Inter-strain variability in the photosynthetic use of inorganic carbon, exemplified by the pH compensation point, in the cyanobacterium Microcystis aeruginosa. Aquat Bot 85: 159-162.
Bapteste, E., Susko, E., Leigh, J., Ruiz-Trillo, I., Bucknam, J., and Doolittle, W. (2007) Alternative methods for concatenation of Core genes indicate a lack of resolution in deep nodes of the prokaryotic phylogeny. Mol Biol Evol 25: 83-91.
Barchewitz, T., Guljamow, A., Meissner, S., Timm, S., Henneberg, M., Baumann, O., et al. (2019) Non-canonical localization of RubisCO under high-light conditions in the toxic cyanobacterium Microcystis aeruginosa PCC7806. Environ Microbiol 21: 4836-4851.
Bastviken, D.T.E., Caraco, N.F., and Cole, J.J. (1998) Experimental measurements of zebra mussel (Dreissena polymorpha) impacts on phytoplankton community composition. Freshw Biol 39: 375-386.
Batista, A.M.M., Woodhouse, J.N., Grossart, H.P., and Giani, A. (2019) Methanogenic archaea associated to Microcystis sp. in field samples and in culture. Hydrobiologia 831: 163-172.
Bayer, B., Pelikan, C., Bittner, M.J., Reinthaler, T., Könneke, M., Herndl, G.J., and Offre, P. (2019) Proteomic response of three marine ammonia-oxidizing archaea to hydrogen peroxide and their metabolic interactions with a heterotrophic Alphaproteobacterium. mSystems 4: 1-15.
Beardall, J., Stojkovic, S., and Larsen, S. (2009) Living in a high CO2 world: impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2: 191-205.
Berry, M.A., Davis, T.W., Cory, R.M., Duhaime, M.B., Johengen, T.H., Kling, G.W., et al. (2017) Cyanobacterial harmful algal blooms are a biological disturbance to Western Lake Erie bacterial communities. Environ Microbiol 19: 1149-1162.
Beversdorf, L.J., Miller, T.R., and McMahon, K.D. (2015) Long-term monitoring reveals carbon-nitrogen metabolism key to microcystin production in eutrophic lakes. Front Microbiol 6: 456.
Biller, S.J., Berube, P.M., Lindell, D., and Chisholm, S.W. (2015) Prochlorococcus: the structure and function of collective diversity. Nat Rev Microbiol 13: 13-27.
Bittencourt-oliveira, M.C., Oliveira, M.C., and Bolch, C.J.S. (2001) Genetic variability of Brazilian strains of the Microcystis aeruginosa complex (Cyanobacteria/Cyanophyceae) using the phycocyanin intergenic spacer and flanking regions (cpcBA). J Phycol 818: 810-818.
Bobay, L.M., and Ochman, H. (2017) The evolution of bacterial genome architecture. Front Genet 8: 1-6.
Bouaïcha, N., Miles, C.O., Beach, D.G., Labidi, Z., Djabri, A., Benayache, N.Y., and Nguyen-quang, T. (2019) Structural diversity, characterization and toxicoloty of microcystins. Toxins (Basel) 11: 1-40.
Bouchard, J.N., and Purdie, D.A. (2011) Effect of elevated temperature, darkness, and hydrogen peroxide treatment on oxidative stress and cell death in the bloom-forming toxic cyanobacterium Microcystis aeruginosa. J Phycol 47: 1316-1325.
Bozarth, C.S., Schwartz, A.D., Shepardson, J.W., Colwell, F.S., and Dreher, T.W. (2010) Population turnover in a Microcystis bloom results in predominantly nontoxigenic variants late in the season. Appl Environ Microbiol 76: 5207-5213.
Brandenburg, K.M., Wohlrab, S., John, U., Kremp, A., Jerney, J., Krock, B., and Van de Waal, D.B. (2018) Intraspecific trait variation and trade-offs within and across populations of a toxic dinoflagellate. Ecol Lett 21: 1561-1571.
Bratbak, G., Egge, J.K., and Heldal, M. (1993) Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93: 39-48.
Breitbart, M. (2012) Marine viruses: truth or dare. Ann Rev Mar Sci 4: 425-448.
Briand, E., Bormans, M., Gugger, M., Dorrestein, P., and Gerwick, W. (2016) Changes in secondary metabolic profiles of Microcystis aeruginosa strains in response to intraspecific interactions. Environ Microbiol 18: 384-400.
Briand, E., Bormans, M., Quiblier, C., Salençon, M.J., and Humbert, J.F. (2012) Evidence of the cost of the production of microcystins by Microcystis aeruginosa under differing light and nitrate environmental conditions. PLoS One 7: e29981.
Briand, E., Escoffier, N., Straub, C., Sabart, M., Quiblier, C., and Humbert, J.F. (2009) Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (cyanobacteria) population. ISME J 3: 419-429.
Briand, E., Reubrecht, S., Mondeguer, F., Sibat, M., Hess, P., Amzil, Z., and Bormans, M. (2019) Chemically mediated interactions between Microcystis and Planktothrix: impact on their growth, morphology and metabolic profiles. Environ Microbiol 21: 1552-1566.
Brookes, J.D. (2001) Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. J Plankton Res 23: 1399-1411.
Brookes, J.D., Regel, R.H., and Ganf, G.G. (2003) Changes in the photo-chemistry of Microcystis aeruginosa in response to light and mixing. New Phytol 158: 151-164.
Brum, J.R., and Sullivan, M.B. (2015) Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat Rev Microbiol 13: 147-159.
Brunberg, A.K. (1999) Contribution of bacteria in the mucilage of Microcystis spp. (cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol Ecol 29: 13-22.
Bui, T., Dao, T.S., Vo, T.G., and Lürling, M. (2018) Warming affects growth rates and microcystin production in tropical bloom-forming Microcystis strains. Toxins (Basel) 10: 123.
Burberg, C., Ilić, M., Petzoldt, T., and von Elert, E. (2019) Nitrate determines growth and protease inhibitor content of the cyanobacterium Microcystis aeruginosa. J Appl Phycol 31: 1697-1707.
Burns, C.W. (1968) The relationship between body size of filter-feeding Cladocera and the maximum size of particle ingested. Limnol Oceanogr 13: 675-678.
Cai, H., Jiang, H., Krumholz, L.R., and Yang, Z. (2014) Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS One 9: e102879.
Caiola, M.G., and Pellegrini, S. (1984) Lysis of Microcystis aeruginosa (Kütz) by Bdellovibrio-like Bacteria. J Phycol 20: 471-475.
Carmichael, W.W. (1992) Cyanobacteria secondary metabolites - the cyanotoxins. J Appl Bacteriol 72: 445-459.
Carmichael, W.W., and Gorham, P. (1981) The Mosaic Nature of Toxic Blooms of Cyanobacteria. In The Water Environment. Boston, MA: Environmental Science Research.
Cataldo, D., Vinocur, A., O′Farrell, I., Paolucci, E., Leites, V., and Boltovskoy, D. (2012) The introduced bivalve Limnoperna fortunei boosts Microcystis growth in Salto Grande reservoir (Argentina): evidence from mesocosm experiments. Hydrobiologia 680: 25-38.
Chaffin, J.D., Davis, T.W., Smith, D.J., Baer, M.M., and Dick, G.J. (2018) Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production. Harmful Algae 73: 84-97.
Chan, J.Z.M., Halachev, M.R., Loman, N.J., Constantinidou, C., and Pallen, M.J. (2012) Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol 12: 302.
Chase, J.M., and Leibold, M.A. (2003) Ecological Niches: Linking Classical and Contemporary Approaches. Chicago: University of Chicago.
Chernoff, N., Hill, D., Lang, J., Schmid, J., Le, T., Farthing, A., and Huang, H. (2020) The comparative toxicity of 10 microcystin congeners administered orally to mice: clinical effects and organ toxicity. Toxins (Basel) 12: 1-18.
Chia, M.A., Jankowiak, J.G., Kramer, B.J., Goleski, J.A., Huang, I.S., Zimba, P.V., et al. (2018) Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions. Harmful Algae 74: 67-77.
Chislock, M.F., Sarnelle, O., Jernigan, L.M., and Wilson, A.E. (2013) Do high concentrations of microcystin prevent Daphnia control of phytoplankton? Water Res 47: 1961-1970.
Chorus, I. (2001) Cyanotoxins - Occurrence, Causes, Consequences. Cham, Switzerland: Springer-Verlag.
Christie-Oleza, J.A., Sousoni, D., Lloyd, M., Armengaud, J., and Scanlan, D.J. (2017) Nutrient recycling facilitates long-term stability of marine microbial phototroph-heterotroph interactions. Nat Microbiol 2: 17100.
Chu, Z., Jin, X., Iwami, N., and Inamori, Y. (2007) The effect of temperature on growth characteristics and competitions of Microcystis aeruginosa and Oscillatoria mougeotii in a shallow, eutrophic lake simulator system. Hydrobiologia 581: 217-223.
Chun, S.J., Cui, Y., Lee, J.J., Choi, I.C., Oh, H.M., and Ahn, C.Y. (2020) Network analysis reveals succession of Microcystis genotypes accompanying distinctive microbial modules with recurrent patterns. Water Res 170: 115326.
Cook, K.V., Li, C., Cai, H., Krumholz, L.R., Hambright, K.D., Paerl, H.W., et al. (2020) The global Microcystis interactome. Limnol Oceanogr 65: S194-S207.
Cooper, W.J., Lean, D.R.S., and Carey, J.H. (1989) Spatial and temporal patterns of hydrogen peroxide in lake waters. Can J Fish Aquat Sci 46: 1227-1231.
Cory, R.M., Davis, T.W., Dick, G.J., Johengen, T., Denef, V.J., Berry, M.A., et al. (2016) Seasonal dynamics in dissolved organic matter, hydrogen peroxide, and cyanobacterial blooms in Lake Erie. Front Mar Sci 3: 1-17.
Cosgrove, K., Coutts, G., Jonsson, I.M., Tarkowski, A., Kokai-Kun, J.F., Mond, J.J., and Foster, S.J. (2007) Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189: 1025-1035.
Costas, E., López-Rodas, V., Toro, F.J., and Flores-Moya, A. (2008) The number of cells in colonies of the cyanobacterium Microcystis aeruginosa satisfies Benford's law. Aquat Bot 89: 341-343.
Cottingham, K.L., Glaholt, S., and Brown, A.C. (2004) Zooplankton community structure affects how phytoplankton respond to nutrient pulses. Ecology 85: 158-171.
Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J., and Smith, A.G. (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438: 90-93.
Davis, T.W., Berry, D.L., Boyer, G.L., and Gobler, C.J. (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8: 715-725.
Davis, T.W., Bullerjahn, G.S., Tuttle, T., McKay, R.M., and Watson, S.B. (2015) Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during Planktothrix blooms in Sandusky Bay, Lake Erie. Environ Sci Technol 49: 7197-7207.
Davis, T.W., Harke, M.J., Marcoval, M.A., Goleski, J., Orano-Dawson, C., Berry, D.L., and Gobler, C.J. (2010) Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquat Microb Ecol 61: 149-162.
Deblois, C.P., and Juneau, P. (2012) Comparison of resistance to light stress in toxic and non-toxic strains of Microcystis aeruginosa (cyanophyta). J Phycol 48: 1002-1011.
Denef, V.J., Kalnejais, L.H., Mueller, R.S., Wilmes, P., Baker, B.J., Thomas, B.C., et al. (2010) Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci U S A 107: 2383-2390.
des Aulnoies, M.G., Roux, P., Caruana, A., Réveillon, D., Briand, E., Hervé, F., et al. (2019) Physiological and metabolic responses of freshwater and brackish-water strains of Microcystis aeruginosa acclimated to a salinity gradient: insight into salt tolerance. Appl Environ Microbiol 85: 1-15.
Díaz, S., Hodgson, J.G., Thompson, K., Cabido, M., Cornelissen, J.H.C., Jalili, A., et al. (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15: 295-304.
Dick, G.J. (2018) Genomic Approaches in Earth and Environmental Sciences. Oxford, UK: Wiley.
Dittmann, E., Gugger, M., Sivonen, K., and Fewer, D.P. (2015) Natural product biosynthetic diversity and comparative genomics of the cyanobacteria. Trends Microbiol 23: 642-652.
Donald, D.B., Bogard, M.J., Finlay, K., and Leavitt, P.R. (2011) Comparative effects of urea, ammonium, and nitrate on phytoplankton abundance, community composition, and toxicity in hypereutrophic freshwaters. Limnol Oceanogr 56: 2161-2175.
Dong, J., Li, C., Chang, M., Dai, D., Liu, S., Quan, B., et al. (2019) Effects of toxic cyanobacterium Microcystis aeruginosa on the morphology of green alga Chlorella vulgaris. Ann Limnol - Int J Limnol 55: 7.
Downing, T.G., Meyer, C., Gehringer, M.M., and Van De Venter, M. (2005) Microcystin content of Microcystis aeruginosa is modulated by nitrogen uptake rate relative to specific growth rate or carbon fixation rate. Environ Toxicol 20: 257-262.
Drábková, M., Admiraal, W., and Maršálek, B. (2007) Combined exposure to hydrogen peroxide and light-selective effects on cyanobacteria, green algae, and diatoms. Environ Sci Technol 41: 309-314.
Droop, M. (1973) Some thoughts on nutrient limitation in algae. J Phycol 9: 264-272.
Duan, Z., Tan, X., Parajuli, K., Upadhyay, S., Zhang, D., Shu, X., and Liu, Q. (2018) Colony formation in two Microcystis morphotypes: effects of temperature and nutrient availability. Harmful Algae 72: 14-24.
Durham, B.P., Dearth, S.P., Sharma, S., Amin, S.A., Smith, C.B., Campagna, S.R., et al. (2017) Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system. Environ Microbiol 19: 3500-3513.
Durham, B.P., Sharma, S., Luo, H., Smith, C.B., Amin, S.A., Bender, S.J., et al. (2015) Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci U S A 112: 453-457.
Dziallas, C., and Grossart, H.P. (2011) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS One 6: e25569.
Ehrenreich, I.M., Waterbury, J.B., and Webb, E.A. (2005) Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes. Appl Environ Microbiol 71: 7401-7413.
Errera, R.M., Yvon-Lewis, S., Kessler, J.D., and Campbell, L. (2014) Reponses of the dinoflagellate Karenia brevis to climate change: PCO2 and sea surface temperatures. Harmful Algae 37: 110-116.
Flynn, K.J., Raven, J.A., Alwyn, T., Rees, T., Finkel, Z., Quigg, A., and Beardall, J. (2010) Is the growth rate hypothesis applicable to microalgae. J Phycol 46: 1-12.
Fogg, G.E. (1991) Tansley review .30. The phytoplanktonic ways of life. New Phytol 118: 191-232.
Follows, M.J., and Dutkiewicz, S. (2011) Modeling diverse communities of marine microbes. Ann Rev Mar Sci 3: 427-451.
Fontana, S., Thomas, M.K., Reyes, M., and Pomati, F. (2019) Light limitation increases multidimensional trait evenness in phytoplankton populations. ISME J 13: 1159-1167.
Forni, C., Telo, F.R., and Caiola, M.G. (1997) Comparative analysis of the polysaccharides produced by different species of Microcystis (Chroococcales, Cyanophyta). Phycologia 36: 181-185.
Frenken, T., Wierenga, J., van Donk, E., Declerck, S.A.J., de Senerpont Domis, L.N., Rohrlack, T., and Van de Waal, D.B. (2018) Fungal parasites of a toxic inedible cyanobacterium provide food to zooplankton. Limnol Oceanogr 63: 2384-2393.
Fuhrman, J.A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541-548.
Gao, K., Helbling, E.W., Häder, D.P., and Hutchins, D.A. (2012) Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar Ecol Prog Ser 470: 167-189.
Ger, K.A., Naus-Wiezer, S., De Meester, L., and Lürling, M. (2019) Zooplankton grazing selectivity regulates herbivory and dominance of toxic phytoplankton over multiple prey generations. Limnol Oceanogr 64: 1214-1227.
Ger, K.A., and Panosso, R. (2014) The effects of a microcystin-producing and lacking strain of Microcystis on the survival of a widespread tropical copepod (Notodiaptomus iheringi). Hydrobiologia 738: 61-73.
Ger, K.A., Urrutia-Cordero, P., Frost, P.C., Hansson, L.A., Sarnelle, O., Wilson, A.E., and Lürling, M. (2016) The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae 54: 128-144.
Gerloff, G., and Skoog, F. (1954) Cell contents of nitrogen and phosphorous as a measure of their availability for growth of Microcystis aeruginosa. Ecology 35: 348-353.
Gerphagnon, M., Latour, D., Colombet, J., and Sime-Ngando, T. (2013) Fungal parasitism: life cycle, dynamics, and impact on Cyanobacterial blooms. PLoS One 8: e60894.
Giordano, M., Beardall, J., and Raven, J.A. (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131.
Gleason, F.H., Jephcott, T.G., Küpper, F.C., Gerphagnon, M., Sime-Ngando, T., Karpov, S.A., et al. (2015) Potential roles for recently discovered chytrid parasites in the dynamics of harmful algal blooms. Fungal Biol Rev 29: 20-33.
Glibert, P.M. (2016) Margalef revisited: a new phytoplankton mandala incorporating twelve dimensions, including nutritional physiology. Harmful Algae 55: 25-30.
Glibert, P.M. (2020) Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae 91: 101583.
Gobler, C.J., Burkholder, J.A.M., Davis, T.W., Harke, M.J., Johengen, T., Stow, C.A., and Van de Waal, D.B. (2016) The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54: 87-97.
Grossart, H.P., and Simon, M. (2007) Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquat Microb Ecol 47: 163-176.
Gu, B., Schelske, C.L., and Coveney, M.F. (2011) Low carbon dioxide partial pressure in a productive subtropical lake. Aquat Sci 73: 317-330.
Guan, D.X., Wang, X., Xu, H., Chen, L., Li, P., and Ma, L.Q. (2018) Temporal and spatial distribution of Microcystis biomass and genotype in bloom areas of Lake Taihu. Chemosphere 209: 730-738.
Harke, M.J., Davis, T.W., Watson, S.B., and Gobler, C.J. (2016a) Nutrient-controlled niche differentiation of Western Lake Erie Cyanobacterial populations revealed via metatranscriptomic surveys. Environ Sci Technol 50: 604-615.
Harke, M.J., and Gobler, C.J. (2013) Global transcriptional responses of the toxic Cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS One 8: e69834.
Harke, M.J., and Gobler, C.J. (2015) Daily transcriptome changes reveal the role of nitrogen in controlling microcystin synthesis and nutrient transport in the toxic cyanobacterium, Microcystis aeruginosa. BMC Genomics 16: 1-18.
Harke, M.J., Steffen, M.M., Gobler, C.J., Otten, T.G., Wilhelm, S.W., Wood, S.A., and Paerl, H.W. (2016b) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54: 4-20.
Harvey, B.P., Gwynn-Jones, D., and Moore, P.J. (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol 3: 1016-1030.
Healey, F.P. (1980) Slope of the Monod equation as an indicator of advantage in nutrient competition. Microb Ecol 5: 281-286.
Hellweger, F.L., Vick, C., Rückbeil, F., and Bucci, V. (2019) Fresh ideas bloom in gut healthcare to cross-fertilize lake management. Environ Sci Technol 53: 14099-14112.
Hennon, G.M., Morris, J.J., Haley, S.T., Zinser, E.R., Durrant, A.R., Entwistle, E., et al. (2018) The impact of elevated CO2 on Prochlorococcus and microbial interactions with “helper” bacterium Alteromonas. ISME J 12: 520-531.
Hesse, K., and Kohl, J. (2001) Effects of light and nutrient supply on growth and microcystin content of different strains of Microcystis aureginosa. In Cyanotoxins Occur Causes, Consequences. Berlin, Germany: Springer, pp. 104-115.
Hillebrand, H., Steinert, G., Boersma, M., Malzahn, A., Meunier, C.L., Plum, C., and Ptacnik, R. (2013) Goldman revisited: faster-growing phytoplankton has lower N: P and lower stoichiometric flexibility. Limnol Oceanogr 58: 2076-2088.
Ho, J.C., Michalak, A.M., and Pahlevan, N. (2019) Widespread global increase in intense lake phytoplankton blooms since the 1980s. Nature 574: 667-670.
Holm, N.P., and Armstrong, D.E. (1981) Role of nutrient limitation and competition in controlling the populations of Asterionella formosa and Microcystis aeruginosa in semicontinuous culture. Limnol Oceanogr 26: 622-634.
Honjo, M., Matsui, K., Ueki, M., Nakamura, R., Fuhrman, J.A., and Kawabata, Z. (2006) Diversity of virus-like agents killing Microcystis aeruginosa in a hyper-eutrophic pond. J Plankton Res 28: 407-412.
Horst, G.P., Sarnelle, O., White, J.D., Hamilton, S.K., Kaul, R.R.B., and Bressie, J.D. (2014) Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. Water Res 54: 188-198.
Hughes, A.R., Inouye, B.D., Johnson, M.T.J., Underwood, N., and Vellend, M. (2008) Ecological consequences of genetic diversity. Ecol Lett 11: 609-623.
Huisman, J., Codd, G.A., Paerl, H.W., Ibelings, B.W., Verspagen, J.M.H., and Visser, P.M. (2018) Cyanobacterial blooms. Nat Rev Microbiol 16: 471-483.
Huisman, J., Jonker, R.R., Zonneveld, C., and Weissing, F.J. (1999) Competition for light between phytoplankton species: experimental tests of mechanistic theory. Ecology 80: 211-222.
Huisman, J., Matthijs, H.C.P., and Visser, P.M. (2005) Harmful Cyanobacteria. Dordrecht, The Netherlands: Springer.
Humbert, J.F., Barbe, V., Latifi, A., Gugger, M., Calteau, A., Coursin, T., et al. (2013) A tribute to disorder in the genome of the bloom-forming freshwater Cyanobacterium Microcystis aeruginosa. PLoS One 8: e70747.
Humbert, J.F., Duris-Latour, D., Le Berre, B., Giraudet, H., and Salençon, M.J. (2005) Genetic diversity in Microcystis populations of a French storage reservoir assessed by sequencing of the 16S-23S rRNA intergenic spacer. Microb Ecol 49: 308-314.
Jackrel, S.L., Schmidt, K.C., Cardinale, B.J., and Denef, V.J. (2020a) Microbiomes reduce their host's sensitivity to interspecific interactions. MBio 11: 1-11.
Jackrel, S.L., White, J.D., Evans, J.T., Buffin, K., Hayden, K., Sarnelle, O., and Denef, V.J. (2019) Genome evolution and host-microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom-forming Microcystis aeruginosa. Mol Ecol 28: 3994-4011.
Jackrel, S.L., Yang, J.W., Schmidt, K.C., and Denef, V.J. (2020b) Host specificity of microbiome assembly and its fitness effects in phytoplankton. ISME J 15: 774-788.
Jacquet, S., Heldal, M., Iglesias-rodriguez, D., Larsen, A., Wilson, W., and Bratbak, G. (2002) Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquat Microb Ecol 27: 111-124.
Jahnichen, S., Petzoldt, T., and Bennodorf, J. (2001) Evidence for control of microcystin dynamics in Bautzen reservoir (Germany) by cyanobacterial population growth rates and dissolved inorganic carbon. J Am Soc Inf Sci 150: 177-196.
Jankowiak, J., Hattenrath-Lehmann, T., Kramer, B.J., Ladds, M., and Gobler, C.J. (2019) Deciphering the effects of nitrogen, phosphorus, and temperature on cyanobacterial bloom intensification, diversity, and toxicity in western Lake Erie. Limnol Oceanogr 64: 1347-1370.
Jankowiak, J.G., and Gobler, C.J. (2020) The composition and function of microbiomes within Microcystis colonies are significantly different than native bacterial assemblages in two north American Lakes. Front Microbiol 11: 1-26.
Janse, I., Kardinaal, W.E.A., Meima, M., Fastner, J., Visser, P.M., and Zwart, G. (2004) Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Appl Environ Microbiol 70: 3979-3987.
Joung, S.H., Oh, H.M., Ko, S.R., and Ahn, C.Y. (2011) Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung reservoir, Korea. Harmful Algae 10: 188-193.
Jover, L.F., Effier, T.C., Buchan, A., Wihelm, S.W., and Weitz, J.S. (2014) The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat Rev Microbiol 12: 519-528.
Juhel, G., Davenport, J., O'Halloran, J., Culloty, S., Ramsay, R., James, K., et al. (2006) Pseudodiarrhoea in zebra mussels Dreissena polymorpha (Pallas) exposed to microcystins. J Exp Biol 209: 810-816.
Jungmann, D., and Benndorf, J. (1994) Toxicity to Daphnia of a compound extracted from laboratory and natural Microcystis spp., and the role of microcystins. Freshw Biol 32: 13-20.
Kaebernick, M., Rohrlack, T., Christoffersen, K., and Neilan, B.A. (2001) A spontaneous mutant of microcystin biosynthesis: genetic characterization and effect on Daphnia. Environ Microbiol 3: 669-679.
Kane, D.D., Conroy, J.D., Peter Richards, R., Baker, D.B., and Culver, D.A. (2014) Re-eutrophication of Lake Erie: correlations between tributary nutrient loads and phytoplankton biomass. J Great Lakes Res 40: 496-501.
Kappers, F. (1985) Growth kinetics of Cyanobacterium Microcystis aeruginosa. Verh Internat Verein Limnol 22: 2821-2824.
Kardinaal, W.E.A., Tonk, L., Janse, I., Hol, S., Slot, P., Huisman, J., and Visser, P.M. (2007) Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Appl Environ Microbiol 73: 2939-2946.
Kehr, J.C., Picchi, D.G., and Dittmann, E. (2011) Natural product biosyntheses in cyanobacteria: a treasure trove of unique enzymes. Beilstein J Org Chem 7: 1622-1635.
Kim, J.G., Park, S.J., Sinninghe Damsté, J.S., Schouten, S., Rijpstra, W.I.C., Jung, M.Y., et al. (2016) Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proc Natl Acad Sci U S A 113: 7888-7893.
Kim, M., Shin, B., Lee, J., Park, H.Y., and Park, W. (2019) Culture-independent and culture-dependent analyses of the bacterial community in the phycosphere of cyanobloom-forming Microcystis aeruginosa. Sci Rep 9: 1-13.
Kimura, S., Uehara, M., Morimoto, D., Yamanaka, M., Sako, Y., and Yoshida, T. (2018) Incomplete selective sweeps of Microcystis population detected by the leader-end CRISPR fragment analysis in a natural pond. Front Microbiol 9: 425.
Kitchens, C.M., Johengen, H., and Davis, T.W. (2018) Establishing spatial and temporal patterns in Microcystis sediment seed stock viability and their relationship to subsequent bloom development in Western Lake Erie. PLoS One 13: 1-18.
Komárek, J. (2003) Coccoid and colonial Cyanobacteria. In Freshwater Algae of North America. Amsterdam: Elsevier, pp. 59-116.
Kondo, R., Yoshida, T., Yuki, Y., and Hiroishi, S. (2000) DNA - DNA reassociation among a bloom- forming cyanobacterial genus. Microcystis 50: 767-770.
Konstantinidis, K.T., Ramette, A., and Tiedje, J.M. (2006) The bacterial species definition in the genomic era. Philos Trans R Soc B Biol Sci 361: 1929-1940.
Krause, S., Le Roux, X., Niklaus, P. A., Van Bodegom, P. M., Lennon, J. T., Bertilsson, S., et al. (2014). Trait-based approaches for understanding microbial biodiversity and ecosystem functioning. Frontiers in Microbiology, 5, 251http://dx.doi.org/10.3389/fmicb.2014.00251.
Kramer, B.J., Davis, T.W., Meyer, K.A., Rosen, B.H., Goleski, J.A., Dick, G.J., et al. (2018) Nitrogen limitation, toxin synthesis potential, and toxicity of cyanobacterial populations in Lake Okeechobee and the St. Lucie River Estuary, Florida, during the 2016 state of emergency event. PLoS One 13: e0196278.
Krausfeldt, L.E., Farmer, A.T., Castro Gonzalez, H.F., Zepernick, B.N., Campagna, S.R., and Wilhelm, S.W. (2019) Urea is both a carbon and nitrogen source for Microcystis aeruginosa: tracking 13C incorporation at bloom pH conditions. Front Microbiol 10: 1-12.
Kurmayer, R., Christiansen, G., and Chorus, I. (2003) The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Appl Environ Microbiol 69: 787-795.
Legrand, C., Rengefors, K., Fistarol, G.O., and Granéli, E. (2003) Allelopathy in phytoplankton - biochemical, ecological and evolutionary aspects. Phycologia 42: 406-419.
Lehman, P.W., Boyer, G., Hall, C., Waller, S., and Gehrts, K. (2005) Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay estuary, California. Hydrobiologia 541: 87-99.
Lei, L., Li, C., Peng, L., and Han, B.P. (2015) Competition between toxic and non-toxic Microcystis aeruginosa and its ecological implication. Ecotoxicology 24: 1411-1418.
Leibold, M.A. (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am Nat 134: 922-949.
Leibold, M.A., Chase, J.M., Shurin, J.B., and Downing, A.L. (1997) Species turnover and the regulation of trophic structure. Annu Rev Ecol Syst 28: 467-494.
Lemaire, V., Brusciotti, S., van Gremberghe, I., Vyverman, W., Vanoverbeke, J., and De Meester, L. (2012) Genotype×genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia. Evol Appl 5: 168-182.
Lezcano, M., Agha, R., Cirés, S., and Quesada, A. (2019) Spatial-temporal survey of Microcystis oligopeptide chemotypes in reservoirs with dissimilar waterbody features and their relation to genetic variation. Harmful Algae 81: 77-85.
Li, A., and Reidenbach, M.A. (2014) Forecasting decadal changes in sea surface temperatures and coral bleaching within a Caribbean coral reef. Coral Reefs 33: 847-861.
Li, P., Cai, Y., Shi, L., Geng, L., Xing, P., Yu, Y., et al. (2009) Microbial degradation and preliminary chemical characterization of Microcystis exopolysaccharides from a Cyanobacterial water bloom of Lake Taihu. Int Rev Hydrobiol 94: 645-655.
Lima, S.L., and Dill, L.M. (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68: 619-640.
Litchman, E., Klausmeier, C.A., Schofield, O.M., and Falkowski, P.G. (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10: 1170-1181.
Liu, J., Van Oosterhout, E., Faassen, E.J., Lürling, M., Helmsing, N.R., and Van de Waal, D.B. (2016) Elevated pCO2 causes a shift towards more toxic microcystin variants in nitrogen-limited Microcystis aeruginosa. FEMS Microbiol Ecol 92: 1-8.
López-Rodas, V., Costas, E., Bañares, E., García-Villada, L., Altamirano, M., Rico, M., et al. (2006) Analysis of polygenic traits of Microcystis aeruginosa (cyanobacteria) strains by restricted maximum likelihood (REML) procedures: 2. Microcystin net production, photosynthesis and respiration. Phycologia 45: 243-248.
Lürling, M. (2003) Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnol Oceanogr 48: 2214-2220.
Lürling, M., Eshetu, F., Faassen, E.J., Kosten, S., and Huszar, V.L.M. (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58: 552-559.
Lyck, S. (2004) Simultaneous changes in cell quotas of microcystin, chlorophyll a, protein and carbohydrate during different growth phases of a batch culture experiment with Microcystis aeruginosa. J Plankton Res 26: 727-736.
Lynch, M. (2007) The Origins of Genome Architecture. Sunderland, MA, USA: Sinaur Associates.
Lyu, K., Gu, L., Wang, H., Zhu, X., Zhang, L., Sun, Y., et al. (2019) Transcriptomic analysis dissects the mechanistic insight into the Daphnia clonal variation in tolerance to toxic Microcystis. Limnol Oceanogr 64: 272-283.
Ma, L., Calfee, B.C., Morris, J.J., Johnson, Z.I., and Zinser, E.R. (2018) Degradation of hydrogen peroxide at the ocean's surface: the influence of the microbial community on the realized thermal niche of Prochlorococcus. ISME J 12: 473-484.
Makower, A.K., Schuurmans, J.M., Groth, D., Zilliges, Y., Matthijs, H.C.P., and Dittmann, E. (2015) Transcriptomics-aided dissection of the intracellular and extracellular roles of microcystin in Microcystis aeruginosa PCC 7806. Appl Environ Microbiol 81: 544-554.
Manage, P.M., Kawabata, Z., and Nakano, S.I. (2001) Dynamics of cyanophage-like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology 2: 73-78.
Manage, P.M., Kawabata, Z., and Nakano, S.-I. (1999) Seasonal changes in densities of cyanophage infectious to Microcystis aeruginosa in a hypereutrophic pond. Hydrobiologia 411: 211-216.
Mankiewicz-Boczek, J., Jaskulska, A., Pawelcyk, J., Gagala, I., Serwecinska, L., and Dziadek, J. (2016) Cyanophages infection of Microcystis bloom in lowland dam reservoir of Sulejów Poland. Microb Ecol 71: 315-325.
Marinho, M.M., De Oliveira, E., and Azevedo, S.M.F. (2007) Influence of N/P ratio on competitive abilities for nitrogen and phosphorus by Microcystis aeruginosa and Aulacoseira distans. Aquat Ecol 41: 525-533.
Martiny, J.B.H., Jones, S.E., Lennon, J.T., and Martiny, A.C. (2015) Microbiomes in light of traits: a pylogenetic perspective. Science 350: 649-655.
Matthijs, H.C.P., Visser, P.M., Reeze, B., Meeuse, J., Slot, P.C., Wijn, G., et al. (2012) Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res 46: 1460-1472.
Mckindles, K. (2017) The effect of phosphorus and nitrogen limitation on viral infection in Microcystis aeruginosa NIES298 using the cyanophage Ma-LMM01.
McKindles, K.M., Manes, M.A., DeMarco, J.R., McClure, A., McKay, R.M., Davis, T.W., and Bullerjahn, G.S. (2020) Dissolved microcystin release coincident with lysis of a bloom dominated by Microcystis spp. in Western Lake Erie attributed to a novel Cyanophage. Appl Environ Microbiol 86: 1-14.
Meyer, K.A., Davis, T.W., Watson, S.B., Denef, V.J., Berry, M.A., and Dick, G.J. (2017) Genome sequences of lower Great Lakes Microcystis sp. reveal strain-specific genes that are present and expressed in western Lake Erie blooms. PLoS One 12: 1-21.
Michalak, A.M., Anderson, E.J., Beletsky, D., Boland, S., Bosch, N.S., Bridgeman, T.B., et al. (2013) Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc Natl Acad Sci U S A 110: 6448-6452.
Mikalsen, B., Boison, G., Skulberg, O.M., Fastner, J., Davies, W., Gabrielsen, T.M., et al. (2003) Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J Bacteriol 185: 2774-2785.
Mikula, P., Zezulka, S., Jancula, D., and Marsalek, B. (2012) Metabolic activity and membrane integrity changes in Microcystis aeruginosa - new findings on hydrogen peroxide toxicity in cyanobacteria. Eur J Phycol 47: 195-206.
Miller, M.A., Kudela, R.M., Mekebri, A., Crane, D., Oates, S.C., Tinker, M.T., et al. (2010) Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS One 5: 1-11.
Mohamed, Z.A., Hashem, M., and Alamri, S.A. (2014) Growth inhibition of the cyanobacterium Microcystis aeruginosa and degradation of its microcystin toxins by the fungus Trichoderma citrinoviride. Toxicon 86: 51-58.
Moisander, P.H., Lehman, P.W., Ochiai, M., and Corum, S. (2009) Diversity of Microcystis aeruginosa in the Klamath River and San Francisco Bay delta, California USA. Aquat Microb Ecol 57: 19-31.
Monchamp, M.E., Pick, F.R., Beisner, B.E., and Maranger, R. (2014) Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PLoS One 9: e85573.
Morimoto, D., Tominaga, K., Nshimura, Y., Yoshida, N., Kimura, S., Sako, Y., and Yoshida, T. (2019) Cooccurrence of broad- and narrow-host-range viruses infecting the bloom-forming toxic Cyanobacterium Microcystis aeruginosa. Environ Microbiol 85: 1-17.
Morris, J.J. (2015) Black queen evolution: the role of leakiness in structuring microbial communities. Trends Genet 31: 475-482.
Morris, J.J., Johnson, Z.I., Szul, M.J., Keller, M., and Zinser, E.R. (2011) Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean's surface. PLoS One 6: e16805.
Morris, J.J., Kirkegaard, R., Szul, M.J., Johnson, Z.I., and Zinser, E.R. (2008) Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by “helper” heterotrophic bacteria. Appl Environ Microbiol 74: 4530-4534.
Morris, J.J., Lenski, R.E., and Zinser, E.R. (2012) The black queen hypothesis: evolution of dependencies through adaptive gene loss. MBio 3: 1-7.
Mowe, M.A.D., Porojan, C., Abbas, F., Mitrovic, S.M., Lim, R.P., Furey, A., and Yeo, D.C.J. (2015) Rising temperatures may increase growth rates and microcystin production in tropical Microcystis species. Harmful Algae 50: 88-98.
Muraille, E. (2018) Diversity generator mechanisms are essential components of biological systems: the two queen hypothesis. Front Microbiol 9: 223.
Nemergut, D.R., Schmidt, S.K., Fukami, T., O'Neill, S.P., Bilinski, T.M., Stanish, L.F., et al. (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77: 342-356.
Nolan, M.P., and Cardinale, B.J. (2019) Species diversity of resident green algae slows the establishment and proliferation of the cyanobacterium Microcystis aeruginosa. Limnologica 74: 23-27.
O'Neil, J.M., Davis, T.W., Burford, M.A., and Gobler, C.J. (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313-334.
Ohio EPA. (2013) Great Lakes Water Quality Agreement Annex 4 Report.
Ohtake, A., Shirai, M., Aida, T., Mori, N., Harada, K.I., Matsuura, K., et al. (1989) Toxicity of Microcystis species isolated from natural blooms and purification of the toxin. Appl Environ Microbiol 55: 3202-3207.
Olsen, Y. (1989) Evaluation of competitive ability of Staurastrum leutkemuellerii (Chlorophyceae) and Microcystis aeruginosa (Cyanophyceae) under P limitation. J Phycol 25: 486-499.
Olsen, Y., Vadstein, O., Anderson, T., and Jensen, A. (1989) Competition between Staurastrum luetkemuellerii (Chlorophyceae) and Microcystis aeruginosa (Cyanophyceae) under varying modes of phosphate supply. J Phycol 25: 499-508.
Omata, T., Price, G.D., Badger, M.R., Okamura, M., Gohta, S., and Ogawa, T. (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci U S A 96: 13571-13576.
Omidi, A., Esterhuizen-Londt, M., and Pflugmacher, S. (2018) Still challenging: the ecological function of the cyanobacterial toxin microcystin-what we know so far. Toxin Rev 37: 87-105.
Orr, P.T., and Jones, G.J. (1998) Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol Oceanogr 43: 1604-1614.
Ostrowski, M., Cavicchioli, R., Blaauw, M., and Gottschal, J.C. (2001) Specific growth rate plays a critical role in hydrogen peroxide resistance of the marine oligotrophic Ultramicrobacterium Sphingomonas alaskensis strain RB2256. Appl Environ Microbiol 67: 1292-1299.
Otsuka, S., Suda, S., Li, R., Matsumoto, S., and Watanabe, M.M. (2000) Morphological variability of colonies of Microcystis morphospecies in culture. J Gen Appl Microbiol 46: 39-50.
Otsuka, S., Suda, S., Shibata, S., Oyaizu, H., Matsumoto, S., and Watanabe, M.M. (2001) A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the bacteriological code. Int J Syst Evol Microbiol 51: 873-879.
Otten, T.G., Crosswell, J.R., Mackey, S., and Dreher, T.W. (2015) Application of molecular tools for microbial source tracking and public health risk assessment of a Microcystis bloom traversing 300km of the Klamath River. Harmful Algae 46: 71-81.
Otten, T.G., Graham, J.L., Harris, T.D., and Dreher, T.W. (2016) Elucidation of tasteand odor-producing bacteria and toxigenic cyanobacteria in a Midwestern drinking water supply reservoir by shotgun metagenomic analysis. Appl Environ Microbiol 82: 5410-5420.
Otten, T.G., and Paerl, H.W. (2015) Health effects of toxic cyanobacteria in U.S. drinking and recreational waters: our current understanding and proposed direction. Curr Environ Heal Rep 2: 75-84.
Otten, T.G., Paerl, H.W., Dreher, T.W., Kimmerer, W.J., and Parker, A.E. (2017) The molecular ecology of Microcystis sp. blooms in the San Francisco estuary. Environ Microbiol 19: 3619-3637.
Otten, T.G., Xu, H., Qin, B., Zhu, G., and Paerl, H.W. (2012) Spatiotemporal patterns and ecophysiology of toxigenic Microcystis blooms in Lake Taihu, China: implications for water quality management. Environ Sci Technol 46: 3480-3488.
Ou, T., Li, S., Liao, X., and Zhang, Q. (2013) Cultivation and characterization of the MaMV-DC cyanophage that infects bloom-forming cyanobacterium Microcystis aeruginosa. Virol Sin 28: 266-271.
Paerl, H.W., and Huisman, J. (2008) Climate: Blooms like it hot. Science 320: 57-58.
Paerl, H.W., and Huisman, J. (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1: 27-37.
Paerl, H.W., and Otten, T.G. (2013a) Blooms bite the hand that feeds them. Science 342: 433-434.
Paerl, H.W., and Otten, T.G. (2013b) Harmful Cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65: 995-1010.
Paerl, H.W., Otten, T.G., and Kudela, R. (2018) Mitigating the expansion of harmful algal blooms across the freshwater-to-marine continuum. Environ Sci Technol 52: 5519-5529.
Paerl, H.W., Scott, J.T., McCarthy, M.J., Newell, S.E., Gardner, W.S., Havens, K.E., et al. (2016) It takes two to tango: when and where dual nutrient (N & P) reductions are needed to Protect Lakes and downstream ecosystems. Environ Sci Technol 50: 10805-10813.
Park, H.D., Iwami, C., Watanabe, M.F., Harada, K.I., Okino, T., and Hayashi, H. (1998) Temporal variabilities of the concentrations of intra- and extracellular microcystin and toxic Microcystis species in a hypertrophie lake, Lake Suwa, Japan (1991-1994). Environ Toxicol Water Qual 13: 61-72.
Parveen, B., Ravet, V., Djediat, C., Mary, I., Quiblier, C., Debroas, D., and Humbert, J.F. (2013) Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environ Microbiol Rep 5: 716-724.
Paul, B., Dixit, G., Murali, T.S., Satyamoorthy, K., and Hao, W. (2019) Genome-based taxonomic classification. Genome 62: 45-52.
Pearson, L.A., Crosbie, N.D., and Neilan, B.A. (2020) Distribution and conservation of known secondary metabolite biosynthesis gene clusters in the genomes of geographically diverse Microcystis aeruginosa strains. Mar Freshw Res 71: 701-716.
Pearson, L.A., Dittmann, E., Mazmouz, R., Ongley, S.E., D'Agostino, P.M., and Neilan, B.A. (2016) The genetics, biosynthesis and regulation of toxic specialized metabolites of cyanobacteria. Harmful Algae 54: 98-111.
Pearson, L.A., Hisbergues, M., Börner, T., Dittmann, E., and Neilan, B.A. (2004) Inactivation of an ABC transporter gene, mcyH, results in loss of microcystin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Appl Environ Microbiol 70: 6370-6378.
Peng, G., Martin, R.M., Dearth, S.P., Sun, X., Boyer, G.L., Campagna, S.R., et al. (2018) Seasonally relevant cool temperatures interact with N chemistry to increase microcystins produced in lab cultures of Microcystis aeruginosa NIES-843. Environ Sci Technol 52: 4127-4136.
Perelman, A., Uzan, A., Hacohen, D., and Schwarz, R. (2003) Oxidative stress in Synechococcus sp. strain PCC 7942: various mechanisms for H2O2 detoxification with different physiological roles. J Bacteriol 185: 3654-3660.
Pérez-Carrascal, O.M., Terrat, Y., Giani, A., Fortin, N., Greer, C.W., Tromas, N., and Shapiro, B.J. (2019) Coherence of Microcystis species revealed through population genomics. ISME J 13: 2887-2900.
Pérez-Carrascal, O.M., Tromas, N., Terrat, Y., Moreno, E., Giani, A., Marques, L.C.B., et al. (2020) Single-colony sequencing reveals phylosymbiosis, co-phylogeny, and horizontal gene transfer between cyanobacterium Microcystis and its microbiome. Pembelajaran Olah Vokal di Prodi Seni Pertunjuk Univ Tanjungpura Pontianak 28: 1-43.
Pflugmacher, S. (2002) Possible allelopathic effects of cyanotoxins, with reference to microcystin-LR, in aquatic ecosystems. Environ Toxicol 17: 407-413.
Piel, T., Sandrini, G., White, E., Xu, T., Schuurmans, J.M., Huisman, J., and Visser, P.M. (2019) Suppressing cyanobacteria with hydrogen peroxide is more effective at high light intensities. Toxins (Basel) 12: 1-20.
Pires, D.L.M., Ibelings, B.W., Brehm, M., and Van Donk, E. (2005) Comparing grazing on lake seston by Dreissena and Daphnia: lessons for biomanipulation. Microb Ecol 50: 242-252.
Pourcel, C., Touchon, M., Villeriot, N., Vernadet, J.P., Couvin, D., Toffano-Nioche, C., and Vergnaud, G. (2020) CRISPRCasdb a successor of CRISPRdb containing CRISPR arrays and cas genes from complete genome sequences, and tools to download and query lists of repeats and spacers. Nucleic Acids Res 48: D535-D544.
Preece, E.P., Hardy, F.J., Moore, B.C., and Bryan, M. (2017) A review of microcystin detections in estuarine and marine waters: environmental implications and human health risk. Harmful Algae 61: 31-45.
Price, G.D. (2011) Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth Res 109: 47-57.
Price, G.D., Woodger, F.J., Badger, M.R., Howitt, S.M., and Tucker, L. (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci U S A 101: 18228-18233.
Puddick, J., Prinsep, M.R., Wood, S.A., Cary, S.C., and Hamilton, D.P. (2016) Modulation of microcystin congener abundance following nitrogen depletion of a Microcystis batch culture. Aquat Ecol 50: 235-246.
Puddick, J., Prinsep, M.R., Wood, S.A., Kaufononga, S.A.F., Cary, S.C., and Hamilton, D.P. (2014) High levels of structural diversity observed in microcystins from Microcystis CAWBG11 and characterization of six new microcystin congeners. Mar Drugs 12: 5372-5395.
Qin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H.W., and Carmichael, W.W. (2010) A drinking water crisis in Lake Taihu, China: linkage to climatic variability and Lake management. Environ Manag 45: 105-112.
Ramos, V., Morais, J., and Vasconcelos, V.M. (2017) A curated database of cyanobacterial strains relevant for modern taxonomy and phylogenetic studies. Sci Data 4: 1-8.
Rangel, M., Martins, J.C.G., Garcia, A.N., Conserva, G.A.A., Costa-Neves, A., Sant'Anna, C.L., and De Carvalho, L.R. (2014) Analysis of the toxicity and histopathology induced by the oral administration of Pseudanabaena galeata and Geitlerinema splendidum (Cyanobacteria) extracts to mice. Mar Drugs 12: 508-524.
Rantala, A., Fewer, D.P., Hisbergues, M., Rouhiainen, L., Vaitomaa, J., Börner, T., and Sivonen, K. (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci U S A 101: 568-573.
Raven, J.A., Giordano, M., Beardall, J., and Maberly, S.C. (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philos Trans R Soc B Biol Sci 367: 493-507.
Raven, J.A., Gobler, C.J., and Hansen, P.J. (2020) Dynamic CO2 and pH levels in coastal, estuarine, and inland waters: theoretical and observed effects on harmful algal blooms. Harmful Algae 91: 101594.
Reinfelder, J.R. (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Ann Rev Mar Sci 3: 291-315.
Renaud, S.L.B., Pick, F.R., and Fortin, N. (2011) Effect of light intensity on the relative dominance of toxigenic and nontoxigenic strains of Microcystis aeruginosa. Appl Environ Microbiol 77: 7016-7022.
Rendulic, S., Pratik, J., Rosinus, A., Eppinger, M., Barr, C., Lanz, C., et al. (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303: 689-692.
Reynolds, C. (1984) The ecology of freshwater phytoplankton. Cambridge, United Kingdom: Cambridge University Press.
Rhee, G.-Y. (1973) A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. 1. J Phycol 9: 495-506.
Rinehart, K.L., Namikoshi, M., and Choi, B.W. (1994) Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). J Appl Phycol 6: 159-176.
Rinta-Kanto, J.M., Konopko, E.A., DeBruyn, J.M., Bourbonniere, R.A., Boyer, G.L., and Wilhelm, S.W. (2009) Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 8: 665-673.
Rinta-Kanto, J.M., Ouellette, A.J.A., Boyer, G.L., Twiss, M.R., Bridgeman, T.B., and Wilhelm, S.W. (2005) Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environ Sci Technol 39: 4198-4205.
Rinta-Kanto, J.M., and Wilhelm, S.W. (2006) Diversity of microcystin-producing cyanobacteria in spatially isolated regions of Lake Erie. Appl Environ Microbiol 72: 5083-5085.
Sagert, S., and Schubert, H. (2000) Acclimation of Palmaria palmata (Rhodophyta) to light intensity: comparison between artificial and natural light fields. J Phycol 36: 1119-1128.
Salvador, D., Churro, C., and Valério, E. (2016) Evaluating the influence of light intensity in mcyA gene expression and microcystin production in toxic strains of Planktothrix agardhii and Microcystis aeruginosa. J Microbiol Methods 123: 4-12.
Sanchez, K., Huntley, N., Duffy, M.A., and Hunter, M.D. (2019) Toxins or medicines? Phytoplankton diets mediate host and parasite fitness in freshwater system. Proc R Soc B Biol Sci 286: 20182231.
Sandrini, G., Jakupovic, D., Matthijs, H.C.P., and Huisman, J. (2015) Strains of the harmful cyanobacterium Microcystis aeruginosa differ in gene expression and activity of inorganic carbon uptake systems at elevated CO2 levels. Appl Environ Microbiol 81: 7730-7739.
Sandrini, G., Ji, X., Verspagen, J.M.H., Tann, R.P., Slot, P.C., Luimstra, V.M., et al. (2016) Rapid adaptation of harmful cyanobacteria to rising CO2. Proc Natl Acad Sci U S A 113: 9315-9320.
Sandrini, G., Matthijs, H.C.P., Verspagen, J.M.H., Muyzer, G., and Huisman, J. (2014) Genetic diversity of inorganic carbon uptake systems causes variation in CO2 response of the cyanobacterium Microcystis. ISME J 8: 589-600.
Sandrini, G., Piel, T., Xu, T., White, E., Qin, H., Slot, P.C., et al. (2020) Harmful algae sensitivity to hydrogen peroxide of the bloom-forming cyanobacterium Microcystis PCC7806 depends on nutrient availability.
Sarnelle, O., White, J.D., Horst, G.P., and Hamilton, S.K. (2012) Phosphorus addition reverses the positive effect of zebra mussels (Dreissena polymorpha) on the toxic cyanobacterium, Microcystis aeruginosa. Water Res 46: 3471-3478.
Sarnelle, O., Wilson, A.E., Hamilton, S.K., Knoll, L.B., and Raikow, D.F. (2005) Complex interactions between the zebra mussel, Dreissena polymorpha, and the harmful phytoplankter, Microcystis aeruginosa. Limnol Oceanogr 50: 896-904.
Saxton, M.A., Arnold, R.J., Bourbonniere, R.A., McKay, R.M.L., and Wilhelm, S.W. (2012) Plasticity of total and intracellular phosphorus quotas in Microcystis aeruginosa cultures and Lake Erie algal assemblages. Front Microbiol 3: 1-9.
Schatz, D., Keren, Y., Hadas, O., Carmeli, S., Sukenik, A., and Kaplan, A. (2005) Ecological implications of the emergence of non-toxic subcultures from toxic Microcystis strains. Environ Microbiol 7: 798-805.
Schatz, D., Keren, Y., Vardi, A., Sukenik, A., Carmell, S., Borner, T., et al. (2007) Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ Microbiol 9: 965-970.
Scheeline, A., Olson, D.L., Williksen, E.P., Horras, G.A., Klein, M.L., and Larter, R. (1997) The peroxidase-oxidase oscillator and its constituent chemistries. Chem Rev 97: 739-756.
Schlosser, D., and Höfer, C. (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68: 3514-3521.
Schmidt, K.C., Jackrel, S.L., Smith, D.J., Dick, G.J., and Denef, V.J. (2020) Genotype and host microbiome alter competitive interactions between Microcystis aeruginosa and Chlorella sorokiniana. Harmful Algae 99: 101939.
Schuurmans, J.M., Brinkmann, B.W., Makower, A.K., Dittmann, E., Huisman, J., and Matthijs, H.C.P. (2018) Microcystin interferes with defense against high oxidative stress in harmful cyanobacteria. Harmful Algae 78: 47-55.
Schwarzenberger, A., Sadler, T., Motameny, S., Ben-Khalifa, K., Frommoit, P., Altmuller, J., et al. (2014) Deciphering the genetic basis of microcystin tolerance. BMC Genomics 15: 776.
Seaver, L.C., and Imlay, J.A. (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 183: 7182-7189.
Sellner, K.G., Lacouture, R.V., and Parrish, C.R. (1988) Effects of increasing salinity on a cyanobacteria bloom in the potomac river estuary. J Plankton Res 10: 49-61.
Sen, B. (1988) Fungal parasitism of planktonic algae in Shearwater. IV: Parasitic occurrence of a new chytrid species on the blue-green alga Microcystis aeruginosa Kuetz. emend. Elenkin. Arch für Hydrobiol Suppl Monogr Beiträge 79: 177-184.
Seyedsayamdost, M.R., Case, R.J., Kolter, R., and Clardy, J. (2011) The Jekyll-and-Hyde chemistry of phaeobacter gallaeciensis. Nat Chem 3: 331-335.
Shapiro, B.J. (2018) What microbial population genomics has taught us about speciation. In Population Genomics: Microorganisms. Cham, Switzerland: Springer, pp. 31-47.
Shen, H., Niu, Y., Xie, P., Tao, M., and Yang, X. (2011) Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshw Biol 56: 1065-1080.
Shen, H., and Song, L. (2007) Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia 592: 475-486.
Shibata, M., Katoh, H., Sonoda, M., Ohkawa, H., Shimoyama, M., Fukuzawa, H., et al. (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277: 18658-18664.
Shibata, M., Ohkawa, H., Kaneko, T., Fukuzawa, H., Tabata, S., Kaplan, A., and Ogawa, T. (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci U S A 98: 11789-11794.
Shih, P.M., Wu, D., Latifi, A., Axen, S.D., Fewer, D.P., Talla, E., et al. (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci U S A 110: 1053-1058.
Siefert, A., Zillig, K.W., Friesen, M.L., and Strauss, S.Y. (2018) Soil microbial communities alter conspecific and congeneric competition consistent with patterns of field coexistence in three Trifolium congeners. J Ecol 106: 1876-1891.
Siefert, A., Zillig, K.W., Friesen, M.L., and Strauss, S.Y. (2019) Mutualists stabilize the coexistence of Congerneric legumes. Am Nat 193: 200-212.
Sime-Ngando, T. (2012) Phytophlankton chytridiomycosis: fungal parasites of phytoplankton and their imprints on the food web dynamics. Front Microbiol 3: 361.
Singh, S., Rai, P.K., Chau, R., Ravi, A.K., Neilan, B.A., and Asthana, R.K. (2015) Temporal variations in microcystin-producing cells and microcystin concentrations in two fresh water ponds. Water Res 69: 131-142.
Sison-Mangus, M.P., Jiang, S., Tran, K.N., and Kudela, R.M. (2014) Host-specific adaptation governs the interaction of the marine diatom, pseudo-nitzschia and their microbiota. ISME J 8: 63-76.
Smith, D., Tan, J., Powers, M., Lin, X., Davis, T., and Dick, G. (2021) Individual Microcstis colonies harbor distinct bacterial communities that differ by Microcystis oligotype and with time. Environ Microbiol Rep. in press, https://doi.org/10.1111/1462-2920.15514.
Smith, T.E., Stevenson, R.J., Caraco, N.F., and Cole, J.J. (1998) Changes in phytoplankton community structure during the zebra mussel (Dreissena polymorpha) invasion of the Hudson River (New York). J Plankton Res 20: 1567-1579.
Sockett, R.E. (2009) Predatory lifestyle of Bdellovibrio bacteriovorus. Annu Rev Microbiol 63: 523-539.
Sohm, J.A., Ahlgren, N.A., Thomson, Z.J., Williams, C., Moffett, J.W., Saito, M.A., et al. (2016) Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron. ISME J 10: 333-345.
Song, H., Lavoie, M., Fan, X., Tan, H., Liu, G., Xu, P., et al. (2017) Allelopathic interactions of linoleic acid and nitric oxide increase the competitive ability of Microcystis aeruginosa. ISME J 11: 1865-1876.
Sønstebø, J.H., and Rohrlack, T. (2011) Possible implications of Chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix. Appl Environ Microbiol 77: 1344-1351.
Soo, R.M., Woodcroft, B.J., Parks, D.H., Tyson, G.W., and Hugenholtz, P. (2015) Back fromthe dead; the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus. PeerJ 2015: 1-22.
Srivastava, A., Jeong, H., Ko, S.R., Ahn, C.Y., Choi, J.W., Park, Y.I., et al. (2019) Phenotypic niche partitioning and transcriptional responses of Microcystis aeruginosa in a spatially heterogeneous environment. Algal Res 41: 101551.
Staehr, P.A., and Birkeland, M.J. (2006) Temperature acclimation of growth, photosynthesis and respiration in two mesophilic phytoplankton species. Phycologia 45: 648-656.
Steffen, M.M., Belisle, B.S., Watson, S.B., Boyer, G.L., Bourbonniere, R.A., and Wilhelm, S.W. (2015) Metatranscriptomic evidence for co-occurring top-down and bottom-up controls on toxic cyanobacterial communities. Appl Environ Microbiol 81: 3268-3276.
Steffen, M.M., Davis, T.W., McKay, R.M.L., Bullerjahn, G.S., Krausfeldt, L.E., Stough, J.M.A., et al. (2017) Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: linkages between biology and the water supply shutdown of Toledo, OH. Environ Sci Technol 51: 6745-6755.
Steffen, M.M., Li, Z., Effler, T.C., Hauser, L.J., Boyer, G.L., and Wilhelm, S.W. (2012) Comparative Metagenomics of toxic freshwater cyanobacteria bloom communities on two continents. PLoS One 7: 1-9.
Straub, C., Quillardet, P., Vergalli, J., de Marsac, N.T., and Humbert, J.F. (2011) A day in the life of Microcystis aeruginosa strain PCC 7806 as revealed by a transcriptomic analysis. PLoS One 6: e16208.
Stumpf, R.P., Wynne, T.T., Baker, D.B., and Fahnenstiel, G.L. (2012) Interannual variability of cyanobacterial blooms in Lake Erie. PLoS One 7: e42444.
Suominen, S., Brauer, V.S., Rantala-Ylinen, A., Sivonen, K., and Hiltunen, T. (2017) Competition between a toxic and a non-toxic Microcystis strain under constant and pulsed nitrogen and phosphorus supply. Aquat Ecol 51: 117-130.
Suttle, C.A. (2007) Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5: 801-812.
Tan, X., Gu, H., Ruan, Y., Zhong, J., Parajuli, K., and Hu, J. (2019) Effects of nitrogen on interspecific competition between two cell-size cyanobacteria: Microcystis aeruginosa and Synechococcus sp. Harmful Algae 89: 101661.
Taranu, Z.E., Pick, F.R., Creed, I.F., Zastepa, A., and Watson, S.B. (2019) Meteorological and nutrient conditions influence microcystin congeners in freshwaters. Toxins (Basel) 11: 1-21.
Tessier, A.J., and Woodruff, P. (2002) Trading off the ability to exploit rich versus poor food quality. Ecol Lett 5: 685-692.
Thiergart, T., Landan, G., and Martin, W.F. (2014) Concatenated alignments and the case of the disappearing tree. BMC Evol Biol 14: 1-12.
Thomas, M.K., and Litchman, E. (2016) Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria. Hydrobiologia 763: 357-369.
Tillett, D., Dittmann, E., Erhard, M., Von Döhren, H., Börner, T., and Neilan, B.A. (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem Biol 7: 753-764.
Tillett, D., Parker, D.L., and Neilan, B.A. (2001) Detection of Toxigenicity by a probe for the microcystin Synthetase a gene (mcyA) of the Cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNa and Phycocyanin operon (Phycocyanin Intergenic spacer) phylogenies. Appl Environ Microbiol 67: 2810-2818.
Tilman, D., Kilham, S.S., and Kilham, P. (1982) Phytoplankton community ecology: the role of limiting nutrients. Annu Rev Ecol Syst Vol 13: 349-372.
Tomioka, N., Imai, A., and Komatsu, K. (2011) Effect of light availability on Microcystis aeruginosa blooms in shallow hypereutrophic Lake Kasumigaura. J Plankton Res 33: 1263-1273.
Tonk, L., Van De Waal, D.B., Slot, P., Huisman, J., Matthijs, H.C.P., and Visser, P.M. (2008) Amino acid availability determines the ratio of microcystin variants in the cyanobacterium Planktothrix agardhii. FEMS Microbiol Ecol 65: 383-390.
Tooming-Klunderud, A., Mikalsen, B., Kristensen, T., and Jakobsen, K.S. (2008) The mosaic structure of the mcyABC operon in Microcystis. Microbiology 154: 1886-1899.
Tucker, S., and Pollard, P. (2005) Identification of cyanophage Ma-LBP and infection of the cyanobacterium Microcystis aeruginosa from an Australian subtropical lake by the virus. Appl Environ Microbiol 71: 629-635.
Turesson, G. (1922) The species and the variety as ecological units. Hereditas 3: 100-113.
Turrill, W.B. (1946) The ecotype concept. A consideration with appreciation and criticism, especially of recent trends. New Phytol 45: 34-43.
United States Environmental Protection Agency. (1977) Effects of Cyanophage SAM-1 Upon Microcystis aeruginosa. Corvallis, OR: U. S. Corvallis Environmental Research Laboratory.
Van de Waal, D.B., Brandenburg, K.M., Keuskamp, J., Trimborn, S., Rokitta, S., Kranz, S.A., and Rost, B. (2019) Highest plasticity of carbon-concentrating mechanisms in earliest evolved phytoplankton. Limnol Oceanogr Lett 4: 37-43.
Van de Waal, D.B., Smith, V.H., Declerck, S.A.J., Stam, E.C.M., and Elser, J.J. (2014) Stoichiometric regulation of phytoplankton toxins. Ecol Lett 17: 736-742.
Van De Waal, D.B., Verspagen, J.M.H., Finke, J.F., Vournazou, V., Immers, A.K., Kardinaal, W.E.A., et al. (2011) Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J 5: 1438-1450.
Van De Waal, D.B., Verspagen, J.M.H., Lürling, M., Van Donk, E., Visser, P.M., and Huisman, J. (2009) The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecol Lett 12: 1326-1335.
van der Westhuizen, A.J., and Eloff, J.N. (1985) Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta 163: 55-59.
Van Mooy, B.A.S., Hmelo, L.R., Sofen, L.E., Campagna, S.R., May, A.L., Dyhrman, S.T., et al. (2012) Quorum sensing control of phosphorus acquisition in Trichodesmium consortia. ISME J 6: 422-429.
Van Rossum, T., Ferretti, P., Maistrenko, O.M., and Bork, P. (2020) Diversity within species: interpreting strains in microbiomes. Nat Rev Microbiol 18: 491-506.
Van Wichelen, J., van Gremberghe, I., Vanormelingen, P., Debeer, A.E., Leporcq, B., Menzel, D., et al. (2010) Strong effects of amoebae grazing on the biomass and genetic structure of a Microcystis bloom (cyanobacteria). Environ Microbiol 12: 2797-2813.
Van Wichelen, J., Vanormelingen, P., Codd, G.A., and Vyverman, W. (2016) The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists. Harmful Algae 55: 97-111.
Vanderploeg, H.A. (1994) Zooplankgon Particle Selection and Feeding Mechanisms: Boca Raton, FL: Lewis Publishers.
Vanderploeg, H.A., Johengen, T.H., and Liebig, J.R. (2009) Feedback between zebra mussel selective feeding and algal composition affects mussel condition: did the regime changer pay a price for its success? Freshw Biol 54: 47-63.
Vanderploeg, H.A., Liebig, J.R., Carmichael, W.W., Agy, M.A., Johengen, T.H., Fahnenstiel, G.L., and Nalepa, T.F. (2001) Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Can J Fish Aquat Sci 58: 1208-1221.
Vanderploeg, H.A., Nalepa, T.F., Jude, D.J., Mills, E.L., Holeck, K.T., Liebig, J.R., et al. (2002) Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Can J Fish Aquat Sci 59: 1209-1228.
Vanderploeg, H.A., Wilson, A.E., Johengen, T.H., Bressie, J.D., Sarnelle, O., Liebig, J.R., et al. (2013) Role of selective grazing by dreissenid mussels in promoting toxic Microcystis blooms and other changes in phytoplankton composition in the Great Lakes. In Quagga Zebra Mussels Biol Impacts, Control Second Ed. Boca Raton, FL: CRC Press, pp. 509-523.
Varble, A., Meaden, S., Barrangou, R., Westra, E.R., and Marraffini, L.A. (2019) Recombination between phages and CRISPR−cas loci facilitates horizontal gene transfer in staphylococci. Nat Microbiol 4: 956-963.
Verspagen, J.M.H., Van de Waal, D.B., Finke, J.F., Visser, P.M., and Huisman, J. (2014) Contrasting effects of rising CO2 on primary production and ecological stoichiometry at different nutrient levels. Ecol Lett 17: 951-960.
Vezie, C., Brient, L., Sivonen, K., Bertru, G., Lefeuvre, J.-C., and Salkinoja-Salonen, M. (1998) Variation of microcystin content of Cyanobacterial blooms and isolated strains in Lake grand-lieu (France). Microb Ecol 35: 126-135.
Vézie, C., Rapala, J., Vaitomaa, J., Seitsonen, J., and Sivonen, K. (2002) Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microb Ecol 43: 443-454.
Via-Ordorika, L., Fastner, J., Kurmayer, R., Hisbergues, M., Dittmann, E., Komarek, J., et al. (2004) Distribution of microcystin-producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies. Syst Appl Microbiol 27: 592-602.
Visser, P.M., Verspagen, J.M.H., Sandrini, G., Stal, L.J., Matthijs, H.C.P., Davis, T.W., et al. (2016) How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 54: 145-159.
Waajen, G.W.A.M., Van Bruggen, N.C.B., Pires, L.M.D., Lengkeek, W., and Lürling, M. (2016) Biomanipulation with quagga mussels (Dreissena rostriformis bugensis) to control harmful algal blooms in eutrophic urban ponds. Ecol Eng 90: 141-150.
Wagg, C., Jansa, J., Stadler, M., Schmid, B., and Van Der Heijden, M.G.A. (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92: 1303-1313.
Wagner, N.D., Osburn, F.S., Wang, J., Taylor, R.B., Boedecker, A.R., Chambliss, C.K., et al. (2019) Biological stoichiometry regulates toxin production in Microcystis aeruginosa (UTEX 2385). Toxins (Basel) 11: 601.
Wang, J., Bai, P., Li, Q., Lin, Y., Huo, D., Ke, F., et al. (2019) Interaction between cyanophage MaMV-DC and eight Microcystis strains, revealed by genetic defense systems. Harmful Algae 85: 101699.
Wang, X., Sun, M., Xie, M., Liu, M., Luo, L., Li, P., and Kong, F. (2013) Differences in microcystin production and genotype composition among Microcystis colonies of different sizes in Lake Taihu. Water Res 47: 5659-5669.
Wantabe, M., and Oishi, S. (1985) Effects of environmental factors on toxicity of a Cyanobacterium (Microcystis aeruginosa) under culture conditions. Microbiology 49: 1342-1344.
Wariishi, H., Valli, K., and Gold, M.H. (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267: 23688-23695.
Webster, K.E., and Peters, R.H. (1978) Some size-dependent inhibitions of larger cladoceran filterers in filamentous suspensions. Limnol Oceanogr 23: 1238-1245.
Weisbrod, B., Riehle, E., Helmer, M., Martin-Creuzburg, D., and Dietrich, D.R. (2020) Can toxin warfare against fungal parasitism influence short-term Dolichospermum bloom dynamics? - a field observation. Harmful Algae 99: 101915.
Welker, M., Maršálek, B., Šejnohová, L., and von Döhren, H. (2006) Detection and identification of oligopeptides in Microcystis (cyanobacteria) colonies: toward an understanding of metabolic diversity. Peptides 27: 2090-2103.
Welker, M., Šejnohová, L., Némethová, D., Von Döhren, H., Jarkovský, J., and Maršálek, B. (2007) Seasonal shifts in chemotype composition of Microcystis sp. communities in the pelagial and the sediment of a shallow reservoir. Limnol Oceanogr 52: 609-619.
Werner, E.E., and Peacor, S.D. (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1083-1100.
White, J.D., Kaul, R.R.B., Knoll, L.B., Wilson, A.E., and Sarnellea, O. (2011) Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnol Oceanogr 56: 1714-1724.
White, J.D., and Sarnelle, O. (2014) Size-structured vulnerability of the colonial cyanobacterium, Microcystis aeruginosa, to grazing by zebra mussels (Dreissena polymorpha). Freshw Biol 59: 514-525.
Whitehead, A., and Crawford, D.L. (2006) Neutral and adaptive variation in gene expression. Proc Natl Acad Sci U S A 103: 5425-5430.
Whitham, T.G., Bailey, J.K., Schweitzer, J.A., Shuster, S.M., Bangert, R.K., Leroy, C.J., et al. (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7: 510-523.
Wiedner, C., Visser, P.M., Fastner, J., Metcalf, J.S., Codd, G.A., and Mur, L.R. (2003) Effects of light on the microcystin content of Microcystis. Appl Environ Microbiol 69: 1475-1481.
Wilhelm, S.W., and Boyer, G.L. (2011) Ecology: healthy competition. Nat Clim Chang 1: 300-301.
Willis, A., and Woodhouse, J.N. (2020) Defining Cyanobacterial species: diversity and description through genomics. CRC Crit Rev Plant Sci 39: 101-124.
Wilson, A.E., Kaul, R.R.B., and Sarnelle, O. (2010) Growth rate consequences of coloniality in a harmful phytoplankter. PLoS One 5: e8679.
Wilson, A.E., Sarnelle, O., Neilan, B.A., Salmon, T.P., Gehringer, M.M., and Hay, M.E. (2005) Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among lakes: implications for harmful algal blooms. Appl Environ Microbiol 71: 6126-6133.
Wilson, A.E., Sarnelle, O., and Tillmanns, A.R. (2006) Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol Oceanogr 51: 1915-1924.
Wommack, K.E., and Colwell, R.R. (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64: 69-114.
Worm, J., and Søndergaard, M. (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (cyanobacteria). Aquat Microb Ecol 14: 19-28.
Wu, S., Mi, T., Zhen, Y., Yu, K., Wang, F., and Yu, Z. (2021) A rise in ROS and EPS production: new insights into the Trichodesmium erythraeum response to ocean acidification. J Phycol 182: 172-182.
Wu, Y., Gao, K., and Riebesell, U. (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7: 2915-2923.
Xiao, M., Li, M., and Reynolds, C.S. (2018) Colony formation in the cyanobacterium Microcystis. Biol Rev 93: 1399-1420.
Xiao, M., Willis, A., and Burford, M.A. (2017) Differences in cyanobacterial strain responses to light and temperature reflect species plasticity. Harmful Algae 62: 84-93.
Xiao, Y., Gan, N., Liu, J., Zheng, L., and Song, L. (2012) Heterogeneity of buoyancy in response to light between two buoyant types of cyanobacterium Microcystis. Hydrobiologia 679: 297-311.
Xu, Z., Te, S.H., He, Y., and Gin, K.Y.H. (2018) The characteristics and dynamics of cyanobacteria-heterotrophic bacteria between two estuarine reservoirs - tropical versus subtropical regions. Front Microbiol 9: 1-13.
Yang, F., Jin, H., Wang, X.-Q., Li, Q., Zhang, J.-T., Cui, N., et al. (2020) Genomic analysis of Mic1 reveals a novel freshwater long-tailed Cyanophage. Front Microbiol 11: 484.
Yang, J., Tang, H., Zhang, X., Zhu, X., Huang, Y., and Yang, Z. (2018) High temperature and pH favor Microcystis aeruginosa to outcompete Scenedesmus obliquus. Environ Sci Pollut Res 25: 4794-4802.
Yang, Z., Kong, F., Shi, X., and Cao, H. (2006) Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563: 225-230.
Yang, Z., Kong, F., Shi, X., Yu, Y., and Zhang, M. (2015) Effects of UV-B radiation on microcystin production of a toxic strain of Microcystis aeruginosa and its competitiveness against a non-toxic strain. J Hazard Mater 283: 447-453.
Yoshida, M., Yoshida, T., Takashima, Y., Hosoda, N., and Hiroishi, S. (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol Lett 266: 49-53.
Yoshida, T., Kamiji, R., Nakamura, G., Kaneko, T., and Sako, Y. (2014) Membrane-like protein involved in phage adsorption associated with phage-sensitivity in the bloom-forming cyanobacterium Microcystis aeruginosa. Harmful Algae 34: 69-75.
You, J., Mallery, K., Hong, J., and Hondzo, M. (2018) Temperature effects on growth and buoyancy of Microcystis aeruginosa. J Plankton Res 40: 16-28.
Zhai, C., Song, S., Zou, S., Liu, C., and Xue, Y. (2013) The mechanism of competition between two bloom-forming Microcystis species. Freshw Biol 58: 1831-1839.
Zhou, Y., Li, X., Gao, Y., Liu, H., Gao, Y.B., van der Heijden, M.G.A., and Ren, A.Z. (2018) Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct Ecol 32: 1168-1179.
Zilliges, Y., Kehr, J.C., Meissner, S., Ishida, K., Mikkat, S., Hagemann, M., et al. (2011) The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS One 6: e17615.
Zinser, E.R. (2018) The microbial contribution to reactive oxygen species dynamics in marine ecosystems. Environ Microbiol Rep 10: 412-427.
Züst, T., and Agrawal, A.A. (2017) Trade-offs between plant growth and defense against insect Herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 60: 513-534.
Zwart, J.A., Solomon, C.T., and Jones, S.E. (2015) Phytoplankton traits predict ecosystem function in a global set of lakes. Ecology 96: 2257-2264.
تواريخ الأحداث: Date Created: 20210531 Date Completed: 20220317 Latest Revision: 20220317
رمز التحديث: 20221213
DOI: 10.1111/1462-2920.15615
PMID: 34056822
قاعدة البيانات: MEDLINE
الوصف
تدمد:1462-2920
DOI:10.1111/1462-2920.15615