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Testing and optimizing metabarcoding of iDNA from dung beetles to sample mammals in the hyperdiverse Neotropics.

التفاصيل البيبلوغرافية
العنوان: Testing and optimizing metabarcoding of iDNA from dung beetles to sample mammals in the hyperdiverse Neotropics.
المؤلفون: Saranholi BH; Department of Life Sciences, Imperial College London, Ascot, UK.; Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos, Brazil., França FM; School of Biological Sciences, University of Bristol, Bristol, UK.; Graduate Program in Ecology, Biological Sciences Institute, Federal University of Pará, Belém, Pará, Brazil., Vogler AP; Department of Life Sciences, Imperial College London, Ascot, UK.; Department of Life Sciences, Natural History Museum, London, UK., Barlow J; Lancaster Environment Centre, Lancaster University, Lancaster, UK., Vaz de Mello FZ; Departamento de Biologia e Zoologia, Universidade Federal de Mato Grosso, Instituto de Biociências, Cuiabá, MT, Brazil., Maldaner ME; Programa de Pós-Graduação Em Ecologia e Conservação da Biodiversidade (PPGECB), Universidade Federal de Mato Grosso (UFMT), Cuiabá, Brazil., Carvalho E; Programa de Pós-Graduação Em Entomologia, Instituto Nacional de Pesquisas da Amazônia, INPA, Manaus, Amazonas, Brazil., Gestich CC; Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos, Brazil., Howes B; Department of Life Sciences, Imperial College London, Ascot, UK., Banks-Leite C; Department of Life Sciences, Imperial College London, Ascot, UK., Galetti PM Jr; Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos, Brazil.
المصدر: Molecular ecology resources [Mol Ecol Resour] 2024 Jul; Vol. 24 (5), pp. e13961. Date of Electronic Publication: 2024 Apr 22.
نوع المنشور: Journal Article; Evaluation Study
اللغة: English
بيانات الدورية: Publisher: Blackwell Country of Publication: England NLM ID: 101465604 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1755-0998 (Electronic) Linking ISSN: 1755098X NLM ISO Abbreviation: Mol Ecol Resour Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Oxford, England : Blackwell
مواضيع طبية MeSH: Coleoptera*/genetics , Coleoptera*/classification , Mammals*/genetics , Mammals*/classification , DNA Barcoding, Taxonomic*/methods, Animals ; RNA, Ribosomal, 16S/genetics ; RNA, Ribosomal/genetics ; Sequence Analysis, DNA/methods ; Biodiversity ; Metagenomics/methods ; DNA/genetics ; Feces/chemistry
مستخلص: Over the past few years, insects have been used as samplers of vertebrate diversity by assessing the ingested-derived DNA (iDNA), and dung beetles have been shown to be a good mammal sampler given their broad feeding preference, wide distribution and easy sampling. Here, we tested and optimized the use of iDNA from dung beetles to assess the mammal community by evaluating if some biological and methodological aspects affect the use of dung beetles as mammal species samplers. We collected 403 dung beetles from 60 pitfall traps. iDNA from each dung beetle was sequenced by metabarcoding using two mini-barcodes (12SrRNA and 16SrRNA). We assessed whether dung beetles with different traits related to feeding, nesting and body size differed in the number of mammal species found in their iDNA. We also tested differences among four killing solutions in preserving the iDNA and compared the effectiveness of each mini barcode to recover mammals. We identified a total of 50 mammal OTUs (operational taxonomic unit), including terrestrial and arboreal species from 10 different orders. We found that at least one mammal-matching sequence was obtained from 70% of the dung beetle specimens. The number of mammal OTUs obtained did not vary with dung beetle traits as well as between the killing solutions. The 16SrRNA mini-barcode recovered a higher number of mammal OTUs than 12SrRNA, although both sets were partly non-overlapping. Thus, the complete mammal diversity may not be achieved by using only one of them. This study refines the methodology for routine assessment of tropical mammal communities via dung beetle 'samplers' and its universal applicability independently of the species traits of local beetle communities.
(© 2024 John Wiley & Sons Ltd.)
References: Aristophanous, M. (2010). Does your preservative preserve? A comparison of the efficacy of some pitfall trap solutions in preserving the internal reproductive organs of dung beetles. ZooKeys, 34, 1–16.
Axtner, J., Crampton‐Platt, A., Hörig, L. A., Mohamed, A., Xu, C. C., Yu, D. W., & Wilting, A. (2019). An efficient and robust laboratory workflow and tetrapod database for larger scale environmental DNA studies. GigaScience, 8(4), giz029.
Barlow, J., França, F., Gardner, T. A., Hicks, C. C., Lennox, G. D., Berenguer, E., Castello, L., Economo, E. P., Ferreira, J., Guénard, B., Gontijo Leal, C., Isaac, V., Lees, A. C., Parr, C. L., Wilson, S. K., Young, P. J., & Graham, N. A. J. (2018). The future of hyperdiverse tropical ecosystems. Nature, 559(7715), 517–526.
Boessenkool, S., Epp, L. S., Haile, J., Bellemain, E., Edwards, M., Coissac, E., Willerslev, E., & Brochmann, C. (2012). Blocking human contaminant DNA during PCR allows amplification of rare mammal species from sedimentary ancient DNA. Molecular Ecology, 21(8), 1806–1815. https://doi.org/10.1111/j.1365‐294x.2011.05306.x.
Bohmann, K., Evans, A., Gilbert, M. T. P., Carvalho, G. R., Creer, S., Knapp, M., Yu, D. W., & de Bruyn, M. (2014). Environmental DNA for wildlife biology and biodiversity monitoring. Trends in Ecology & Evolution, 29(6), 358–367.
Brocardo, C. B., Rosa, C. A., Sampaio, R., Castro, A. B., Rossi, L. C., Rosa, D. P., Nóbrega, J., & Fadini, R. F. (2022). Mamíferos de médio e grande porte (exceto primatas) da Floresta Nacional do Tapajós e da Reserva Extrativista Tapajós‐Arapiuns. In C. R. Brocardo & L. L. Giacomin (Eds.), Biodiversidade na Floresta Nacional do Tapajós e na Reserva Extrativista Tapajós – Arapiuns (pp. 280–295). UFOPA.
Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Maechler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero‐inflated generalized linear mixed modeling. The R Journal, 9(2), 378–400. https://doi.org/10.32614/RJ‐2017‐066.
Calvignac‐Spencer, S., Leendertz, F. H., Gilbert, M. T. P., & Schubert, G. (2013). An invertebrate stomach's view on vertebrate ecology: Certain invertebrates could be used as “vertebrate samplers” and deliver DNA‐based information on many aspects of vertebrate ecology. BioEssays, 35(11), 1004–1013.
Calvignac‐Spencer, S., Merkel, K., Kutzner, N., Kühl, H., Boesch, C., Kappeler, P. M., Metzger, S., Schubert, G., & Leendertz, F. H. (2013). Carrion fly‐derived DNA as a tool for comprehensive and cost‐effective assessment of mammalian biodiversity. Molecular Ecology, 22(4), 915–924.
Cambefort, Y. (1991). Dung beetles in tropical savannas. In Y. Cambefort & I. Hanski (Eds.), Dung beetle ecology (pp. 156–178). Princeton University Press.
Carvalho, C. S., De Oliveira, M. E., Rodriguez‐Castro, K. G., Saranholi, B. H., & Galetti, P. M., Jr. (2022). Efficiency of eDNA and iDNA in assessing vertebrate diversity and its abundance. Molecular Ecology Resources, 22(4), 1262–1273.
Carvalho, E. C., Maldaner, M., Costa‐Silva, V., Sehn, H., Franquini, C., Campos, V., Seba, V. P., Maia, L. F., Vaz‐de‐Mello, F. Z., & França, F. (2023). Dung beetles from two sustainable‐use protected forests in the Brazilian Amazon. Biodiversity Data Journal, 11, e96101.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124–3140. https://doi.org/10.1111/mec.12354.
Champlot, S., Berthelot, C., Pruvost, M., Bennett, E. A., Grange, T., & Geigl, E. M. (2010). An efficient multistrategy DNA decontamination procedure of PCR reagents for hypersensitive PCR applications. PLoS One, 5(9), e13042.
Chiew, L. Y., Hackett, T. D., Brodie, J. F., Teoh, S. W., Burslem, D. F., Reynolds, G., Deere, N. J., Vairappan, C. S., & Slade, E. M. (2022). Tropical forest dung beetle–mammal dung interaction networks remain similar across an environmental disturbance gradient. Journal of Animal Ecology, 91(3), 604–617.
Correa, C. M., Salomão, R. P., Xavier, B. F., Puker, A., & Ferreira, K. R. (2023). Not all dung beetles feed on dung: Scarabaeinae (Coleoptera: Scarabaeidae) attracted to different carrion types in contrasting habitats at Brazilian Amazon. Austral Ecology, 48, 952–968.
Cristescu, M. E., & Hebert, P. D. (2018). Uses and misuses of environmental DNA in biodiversity science and conservation. Annual Review of Ecology, Evolution, and Systematics, 49, 209–230.
Drinkwater, R., Williamson, J., Clare, E. L., Chung, A. Y., Rossiter, S. J., & Slade, E. (2021). Dung beetles as samplers of mammals in Malaysian Borneo—A test of high throughput metabarcoding of iDNA. PeerJ, 9, e11897.
Edgar, R. (2010). Usearch. Lawrence Berkeley National Lab. (LBNL).
Fahmy, M., Ravelomanantsoa, N. A. F., Youssef, S., Hekkala, E., & Siddall, M. (2019). Biological inventory of Ranomafana National Park tetrapods using leech‐derived iDNA. European Journal of Wildlife Research, 65(5), 1–13.
Frank, K., Krell, F. T., Slade, E. M., Raine, E. H., Chiew, L. Y., Schmitt, T., Vairappan, C. S., Walter, P., & Blüthgen, N. (2018). Global dung webs: High trophic generalism of dung beetles along the latitudinal diversity gradient. Ecology Letters, 21(8), 1229–1236.
Gardner, T. A., Barlow, J., Araujo, I. S., Avila‐Pires, T. C., Bonaldo, A. B., Costa, J. E., Esposito, M. C., Ferreira, L. V., Hawes, J., Hernandez, M. I., Hoogmoed, M. S., Leite, R. N., Lo‐Man‐Hung, N. F., Malcolm, J. R., Martins, M. B., Mestre, L. A., Miranda‐Santos, R., Overal, W. L., Parry, L., … Peres, C. A. (2008). The cost‐effectiveness of biodiversity surveys in tropical forests. Ecology Letters, 11(2), 139–150.
Gillett, C., Johnson, A., Barr, I., & Hulcr, J. (2016). Metagenomic sequencing of dung beetle intestinal contents directly detects and identifies mammalian fauna. bioRxiv. https://doi.org/10.1101/074849.
Gogarten, J. F., Hoffmann, C., Arandjelovic, M., Sachse, A., Merkel, K., Dieguez, P., Agbor, A., Angedakin, S., Brazzola, G., Jones, S., Langergraber, K. E., Lee, K., Marrocoli, S., Murai, M., Sommer, V., Kühl, H., Leendertz, F. H., & Calvignac‐Spencer, S. (2020). Fly‐derived DNA and camera traps are complementary tools for assessing mammalian biodiversity. Environmental DNA, 2(1), 63–76.
Gómez, A., & Kolokotronis, S. O. (2017). Genetic identification of mammalian meal source in dung beetle gut contents. Mitochondrial DNA Part A DNA Mapping, Sequencing, and Analysis, 28(4), 612–615.
Gotelli, N. J., & Colwell, R. K. (2001). Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4(4), 379–391.
Hughes, A. C., Orr, M. C., Ma, K., Costello, M. J., Waller, J., Provoost, P., Yang, Q., Zhu, C., & Qiao, H. (2021). Sampling biases shape our view of the natural world. Ecography, 44(9), 1259–1269.
ICMBio. (2019). Plano de Manejo Floresta Nacional do Tapajós: Volume I ‐ Diagnóstico. https://www.gov.br/icmbio/pt‐br/assuntos/biodiversidade/unidade‐de‐conservacao/unidades‐de‐biomas/amazonia/lista‐de‐ucs/flona‐do‐tapajos.
Keeping, D., & Pelletier, R. (2014). Animal density and track counts: Understanding the nature of observations based on animal movements. PLoS One, 9(5), e96598.
Kelly, R. P., Port, J. A., Yamahara, K. M., Martone, R. G., Lowell, N., Thomsen, P. F., Mach, M. E., Bennett, M., Prahler, E., Caldwell, M. R., & Crowder, L. B. (2014). Harnessing DNA to improve environmental management. Science, 344(6191), 1455–1456.
Kerley, G. I., Landman, M., Ficetola, G. F., Boyer, F., Bonin, A., Rioux, D., Taberlet, P., & Coissac, E. (2018). Diet shifts by adult flightless dung beetles Circellium bacchus, revealed using DNA metabarcoding, reflect complex life histories. Oecologia, 188(1), 107–115.
Kiffner, C., Thomas, S., Speaker, T., O'Connor, V., Schwarz, P., Kioko, J., & Kissui, B. (2020). Community‐based wildlife management area supports similar mammal species richness and densities compared to a national park. Ecology and Evolution, 10(1), 480–492.
Kinoshita, G., Yonezawa, S., Murakami, S., & Isagi, Y. (2019). Environmental DNA collected from snow tracks is useful for identification of mammalian species. Zoological Science, 36(3), 198–207.
Kirtane, A. A., Wilder, M. L., & Green, H. C. (2019). Development and validation of rapid environmental DNA (eDNA) detection methods for bog turtle (Glyptemys muhlenbergii). PLoS One, 14(11), e0222883.
Kocher, A., de Thoisy, B., Catzeflis, F., Huguin, M., Valière, S., Zinger, L., Bañuls, A. L., & Murienne, J. (2017). Evaluation of short mitochondrial metabarcodes for the identification of Amazonian mammals. Methods in Ecology and Evolution, 8(10), 1276–1283.
Leempoel, K., Hebert, T., & Hadly, E. A. (2020). A comparison of eDNA to camera trapping for assessment of terrestrial mammal diversity. Proceedings of the Royal Society B, 287(1918), 20192353.
Lenth, R. (2023). emmeans: Estimated Marginal Means, aka Least‐Squares Means_. R package version 1.8.5. https://CRAN.R‐project.org/package=emmeans.
Lynggaard, C., Nielsen, M., Santos‐Bay, L., Gastauer, M., Oliveira, G., & Bohmann, K. (2019). Vertebrate diversity revealed by metabarcoding of bulk arthropod samples from tropical forests. Environmental DNA, 1(4), 329–341.
Marques, T. A., Thomas, L., Martin, S. W., Mellinger, D. K., Ward, J. A., Moretti, D. J., Harris, D., & Tyack, P. L. (2013). Estimating animal population density using passive acoustics. Biological Reviews, 88(2), 287–309.
Marsh, C. J., Louzada, J., Beiroz, W., & Ewers, R. M. (2013). Optimising bait for pitfall trapping of Amazonian dung beetles (Coleoptera: Scarabaeinae). PLoS One, 8(8), e73147.
Martin, M. (2011). Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet. Journal, 17(1), 10–12.
Massey, A. L., Bronzoni, R. V. M., da Silva, D. J. F., Allen, J. M., de Lázari, P. R., dos Santos‐Filho, M., Canale, G. R., Bernardo, C. S. S., Peres, C. A., & Levi, T. (2022). Invertebrates for vertebrate biodiversity monitoring: Comparisons using three insect taxa as iDNA samplers. Molecular Ecology Resources, 22(3), 962–977. Portico. https://doi.org/10.1111/1755‐0998.13525.
McKee, A. M., Calhoun, D. L., Barichivich, W. J., Spear, S. F., Goldberg, C. S., & Glenn, T. C. (2015). Assessment of environmental DNA for detecting presence of imperiled aquatic amphibian species in isolated wetlands. Journal of Fish and Wildlife Management, 6(2), 498–510. https://doi.org/10.3996/042014‐JFWM‐034.
Medina, A. M., & Lopes, P. P. (2014). Resource utilization and temporal segregation of Scarabaeinae (Coleoptera, Scarabaeidae) community in a Caatinga fragment. Neotropical Entomology, 43, 127–133.
Mora‐Aguilar, E. F., Arriaga‐Jimenez, A., Correa, C. M., da Silva, P. G., Korasaki, V., López‐Bedoya, P. A., Hernández, M. I. M., Pablo‐Cea, J. D., Salomão, R. P., Valencia, G., Vulinec, K., & Noriega, J. A. (2023). Toward a standardized methodology for sampling dung beetles (Coleoptera: Scarabaeinae) in the Neotropics: A critical review. Frontiers in Ecology and Evolution, 11, 1096208.
Nichols, E., & Gardner, T. A. (2011). Dung beetles as a candidate study taxon in applied biodiversity conservation research. In L. W. Simmons, & J. Ridsdill‐Smith (Eds.), Dung Beetle Ecology and Evolution (pp. 267–291). Wiley‐Blackwell.
Nichols, J. D., & Karanth, K. U. (2011). In A. F. O'Connell (Ed.), Camera traps in animal ecology: Methods and analyses (Vol. 271). Springer.
Nimalrathna, T. S., Fan, H., Quan, R. C., & Nakamura, A. (2023). Enhancing the dung beetle iDNA tool for mammalian biodiversity monitoring and ecological studies. Integrative Conservation, 2(3), 133–139.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'hara, R. B., Simpson, G., Solymos, P., Stevenes, M. H. H., & Wagner, H. (2013). Package ‘vegan’. Community ecology package, version, 2(9), 1–295.
Olds, B. P., Jerde, C. L., Renshaw, M. A., Li, Y., Evans, N. T., Turner, C. R., Deiner, K., Mahon, A. R., Brueseke, M. A., Shirey, P. D., Pfrender, M. E., Lodge, D. M., & Lamberti, G. A. (2016). Estimating species richness using environmental DNA. Ecology and Evolution, 6(12), 4214–4226.
Pikitch, E. K. (2018). A tool for finding rare marine species. Science, 360(6394), 1180–1182.
R Development Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Raine, E. H., Mikich, S. B., Lewis, O. T., Riordan, P., Vaz‐de‐Mello, F. Z., & Slade, E. M. (2018). Extinctions of interactions: Quantifying a dung beetle–mammal network. Ecosphere, 9(11), e02491.
Ravetta, A. L., & Brocardo, C. B. (2022). Primatas da Floresta Nacional do Tapajós e da Reserva Extrativista Tapajós‐Arapiuns. In C. R. Brocardo & L. L. Giacomin (Eds.), Biodiversidade na Floresta Nacional do Tapajós e na Reserva Extrativista Tapajós – Arapiuns (pp. 296–309). UFOPA.
Riaz, T., Shehzad, W., Viari, A., Pompanon, F., Taberlet, P., & Coissac, E. (2011). ecoPrimers: Inference of new DNA barcode markers from whole genome sequence analysis. Nucleic Acids Research, 39(21), e145.
Ripple, W. J., Estes, J. A., Beschta, R. L., Wilmers, C. C., Ritchie, E. G., Hebblewhite, M., Berger, J., Elmhagen, B., Letnic, M., Nelson, M. P., Schmitz, O. J., Smith, D. W., Wallach, A. D., & Wirsing, A. J. (2014). Status and ecological effects of the world's largest carnivores. Science, 343(6167), 1241484.
Rodgers, T. W., Xu, C. C., Giacalone, J., Kapheim, K. M., Saltonstall, K., Vargas, M., Yu, D. W., Somervuo, P., McMillan, W., & Jansen, P. A. (2017). Carrion fly‐derived DNA metabarcoding is an effective tool for mammal surveys: Evidence from a known tropical mammal community. Molecular Ecology Resources, 17(6), e133–e145.
Salomão, R. P., Maia, A. C. D., Bezerra, B. M., & Iannuzzi, L. (2018). Attractiveness of different food resources to dung beetles (Coleoptera: Scarabaeidae) of a dry tropical area. Neotropical Entomology, 47, 69–78.
Saranholi, B. H., Rodriguez‐Castro, K. G., Carvalho, C. S., Chahad‐Ehlers, S., Gestich, C. C., Andrade, S. C., Freitas, P. D., & Galetti, P. M., Jr. (2023). Comparing iDNA from mosquitoes and flies to survey mammals in a semi‐controlled Neotropical area. Molecular Ecology Resources, 23, 1790–1799. https://doi.org/10.1111/1755‐0998.13851.
Schnell, I. B., Bohmann, K., & Gilbert, M. T. P. (2015). Tag jumps illuminated–reducing sequence‐to‐sample misidentifications in metabarcoding studies. Molecular Ecology Resources, 15(6), 1289–1303.
Scholtz, C. H., Davis, A. L. V., & Kryger, U. (2009). Evolutionary biology and conservation of dung beetles (pp. 1–567). Pensoft.
Smith, J. A., Suraci, J. P., Hunter, J. S., Gaynor, K. M., Keller, C. B., Palmer, M. S., Atkins, J. L., Castañeda, I., Cherry, M. J., Garvey, P. M., Huebner, S. E., Morin, D. J., Teckentrup, L., Weterings, M. J. A., & Beaudrot, L. (2020). Zooming in on mechanistic predator–prey ecology: Integrating camera traps with experimental methods to reveal the drivers of ecological interactions. Journal of Animal Ecology, 89(9), 1997–2012.
Stavert, J. R., Gaskett, A. C., Scott, D. J., & Beggs, J. R. (2014). Dung beetles in an avian‐dominated island ecosystem: feeding and trophic ecology. Oecologia, 176, 259–271.
Taylor, P. G. (1996). Reproducibility of ancient DNA sequences from extinct Pleistocene fauna. Molecular Biology and Evolution, 13(1), 283–285.
Tonelli, M. (2021). Some considerations on the terminology applied to dung beetle functional groups. Ecological Entomology, 46(4), 772–776.
Varman, K. S., & Sukumar, R. (1995). The line transect method for estimating densities of large mammals in a tropical deciduous forest: An evaluation of models and field experiments. Journal of Biosciences, 20(2), 273–287.
Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2014). PEAR: A fast and accurate Illumina paired‐end reAd mergeR. Bioinformatics, 30(5), 614–620. https://doi.org/10.1093/bioinformatics/btt593.
معلومات مُعتمدة: 1989427 University of Bristol (PolicyBristol, SYNPAM); ProjectBIOCLIMATE BNP Paribas Foundation (Climate and Biodiversity Initiative); 2258319 Cabot Seedcorn 2023 (Voices of Amazonia); 303524/2019-7 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 406767/2022-0 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 420254/2018-8 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 441257/2023-2 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 441573/2020-7 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 441659/2016-0 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 1777136 University of Bristol (Liv Sidse Jansen Memorial Foundation, FOR-TRAITS); NE/S011811/1 Natural Environment Research Council; 170839 Climate and Net Zero Impact Awards (Scaling-up TAOCA); MR/X032949/1 United Kingdom MRC_ Medical Research Council
فهرسة مساهمة: Keywords: Amazonian rain forest; biodiversity; biomonitoring; invertebrate‐derived DNA; metabarcoding
المشرفين على المادة: 0 (RNA, Ribosomal, 16S)
0 (RNA, ribosomal, 12S)
0 (RNA, Ribosomal)
9007-49-2 (DNA)
تواريخ الأحداث: Date Created: 20240422 Date Completed: 20240603 Latest Revision: 20240603
رمز التحديث: 20240603
DOI: 10.1111/1755-0998.13961
PMID: 38646932
قاعدة البيانات: MEDLINE
الوصف
تدمد:1755-0998
DOI:10.1111/1755-0998.13961