دورية أكاديمية
أعرض في EDS

The impact of phage and phage resistance on microbial community dynamics.

التفاصيل البيبلوغرافية
العنوان: The impact of phage and phage resistance on microbial community dynamics.
المؤلفون: Alseth EO; Environment and Sustainability Institute, Biosciences, University of Exeter, Penryn, United Kingdom.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, United States of America.; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America., Custodio R; Environment and Sustainability Institute, Biosciences, University of Exeter, Penryn, United Kingdom., Sundius SA; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, United States of America.; School of Math, Georgia Institute of Technology, Atlanta, Georgia, United States of America.; Interdisciplinary Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America., Kuske RA; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, United States of America.; School of Math, Georgia Institute of Technology, Atlanta, Georgia, United States of America., Brown SP; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, United States of America.; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America., Westra ER; Environment and Sustainability Institute, Biosciences, University of Exeter, Penryn, United Kingdom.
المصدر: PLoS biology [PLoS Biol] 2024 Apr 22; Vol. 22 (4), pp. e3002346. Date of Electronic Publication: 2024 Apr 22 (Print Publication: 2024).
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Public Library of Science Country of Publication: United States NLM ID: 101183755 Publication Model: eCollection Cited Medium: Internet ISSN: 1545-7885 (Electronic) Linking ISSN: 15449173 NLM ISO Abbreviation: PLoS Biol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: San Francisco, CA : Public Library of Science, [2003]-
مواضيع طبية MeSH: Bacteriophages*/physiology , Bacteriophages*/genetics , Pseudomonas aeruginosa*/virology , CRISPR-Cas Systems* , Microbiota*, Acinetobacter baumannii/virology ; Mutation ; Bacteria/virology ; Bacteria/genetics
مستخلص: Where there are bacteria, there will be bacteriophages. These viruses are known to be important players in shaping the wider microbial community in which they are embedded, with potential implications for human health. On the other hand, bacteria possess a range of distinct immune mechanisms that provide protection against bacteriophages, including the mutation or complete loss of the phage receptor, and CRISPR-Cas adaptive immunity. While our previous work showed how a microbial community may impact phage resistance evolution, little is known about the inverse, namely how interactions between phages and these different phage resistance mechanisms affect the wider microbial community in which they are embedded. Here, we conducted a 10-day, fully factorial evolution experiment to examine how phage impact the structure and dynamics of an artificial four-species bacterial community that includes either Pseudomonas aeruginosa wild-type or an isogenic mutant unable to evolve phage resistance through CRISPR-Cas. Additionally, we used mathematical modelling to explore the ecological interactions underlying full community behaviour, as well as to identify general principles governing the impacts of phage on community dynamics. Our results show that the microbial community structure is drastically altered by the addition of phage, with Acinetobacter baumannii becoming the dominant species and P. aeruginosa being driven nearly extinct, whereas P. aeruginosa outcompetes the other species in the absence of phage. Moreover, we find that a P. aeruginosa strain with the ability to evolve CRISPR-based resistance generally does better when in the presence of A. baumannii, but that this benefit is largely lost over time as phage is driven extinct. Finally, we show that pairwise data alone is insufficient when modelling our microbial community, both with and without phage, highlighting the importance of higher order interactions in governing multispecies dynamics in complex communities. Combined, our data clearly illustrate how phage targeting a dominant species allows for the competitive release of the strongest competitor while also contributing to community diversity maintenance and potentially preventing the reinvasion of the target species, and underline the importance of mapping community composition before therapeutically applying phage.
Competing Interests: E.R.W. is inventor on patent GB2303034.9.
(Copyright: © 2024 Alseth et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
التعليقات: Update of: bioRxiv. 2023 Sep 26;:. (PMID: 37808693)
References: Nat Rev Microbiol. 2016 Feb;14(2):93-105. (PMID: 26714431)
Sci Rep. 2018 Jul 17;8(1):10812. (PMID: 30018338)
Nat Rev Gastroenterol Hepatol. 2012 Oct;9(10):599-608. (PMID: 22907164)
Malar J. 2004 Sep 14;3:33. (PMID: 15367331)
Science. 2007 Mar 23;315(5819):1709-12. (PMID: 17379808)
Science. 2019 Mar 29;363(6434):. (PMID: 30923196)
Nat Rev Microbiol. 2020 Mar;18(3):125-138. (PMID: 32015529)
Proc Natl Acad Sci U S A. 2017 Dec 26;114(52):13774-13779. (PMID: 29233945)
Proc Natl Acad Sci U S A. 2015 Jun 16;112(24):7563-8. (PMID: 26041805)
Biofouling. 2013;29(4):457-68. (PMID: 23597188)
Nat Rev Microbiol. 2018 Mar;16(3):143-155. (PMID: 29332945)
Nature. 2016 Apr 21;532(7599):385-8. (PMID: 27074511)
Nat Microbiol. 2016 Aug 22;1(11):16140. (PMID: 27782139)
ISME J. 2014 Jul;8(7):1391-402. (PMID: 24621522)
Nat Rev Genet. 2023 Feb;24(2):109-124. (PMID: 36198908)
PLoS One. 2012 Dec 20;7(12):e53157. (PMID: 23308090)
Cell Rep. 2023 Jul 25;42(7):112672. (PMID: 37347666)
mSphere. 2022 Oct 26;7(5):e0031822. (PMID: 35972133)
Nat Commun. 2016 Aug 02;7:12285. (PMID: 27481625)
Microbiome. 2018 Feb 01;6(1):24. (PMID: 29391057)
Science. 2015 Nov 6;350(6261):663-6. (PMID: 26542567)
BMC Ecol. 2020 Jan 8;20(1):3. (PMID: 31914976)
Philos Trans R Soc Lond B Biol Sci. 2013 Jun 24;368(1623):20120150. (PMID: 23798698)
Curr Biol. 2015 Apr 20;25(8):1043-9. (PMID: 25772450)
Environ Microbiol Rep. 2017 Feb;9(1):33-35. (PMID: 27888577)
Nat Rev Microbiol. 2022 Oct;20(10):579-592. (PMID: 35136217)
Elife. 2013 Nov 05;2:e01202. (PMID: 24192039)
ISME J. 2021 Feb;15(2):534-544. (PMID: 33011743)
Infect Immun. 2014 Aug;82(8):3417-25. (PMID: 24891106)
Proc Natl Acad Sci U S A. 2019 Aug 6;116(32):15979-15984. (PMID: 31270235)
mBio. 2023 Feb 28;14(1):e0134922. (PMID: 36475750)
Cell Host Microbe. 2019 Feb 13;25(2):184-194. (PMID: 30763533)
Nat Rev Microbiol. 2023 Oct;21(10):686-700. (PMID: 37460672)
Nat Chem Biol. 2022 Nov;18(11):1245-1252. (PMID: 36050493)
Sci Rep. 2016 May 26;6:26717. (PMID: 27225966)
Biochem J. 2017 May 16;474(11):1823-1836. (PMID: 28512250)
PLoS One. 2016 Aug 09;11(8):e0160840. (PMID: 27505423)
J Food Prot. 2007 Jan;70(1):90-6. (PMID: 17265865)
Curr Opin Biotechnol. 2021 Apr;68:89-95. (PMID: 33176253)
Mol Syst Biol. 2018 Jun 21;14(6):e8157. (PMID: 29930200)
Clin Microbiol Infect. 2010 Jul;16(7):821-30. (PMID: 20880411)
Mol Ecol. 2018 Apr;27(8):2025-2038. (PMID: 29457297)
Nat Rev Microbiol. 2022 Jan;20(1):49-62. (PMID: 34373631)
Genetics. 1996 May;143(1):15-26. (PMID: 8722758)
Nature. 2017 Oct 5;550(7674):61-66. (PMID: 28953883)
Gut. 2019 Jul;68(7):1169-1179. (PMID: 30842211)
Appl Environ Microbiol. 2008 Jan;74(1):172-81. (PMID: 17981942)
PLoS Comput Biol. 2022 Oct 10;18(10):e1010548. (PMID: 36215322)
Expert Rev Anti Infect Ther. 2013 Mar;11(3):297-308. (PMID: 23458769)
Sci Rep. 2017 Aug 23;7(1):9212. (PMID: 28835692)
Cell. 2015 Jan 29;160(3):447-60. (PMID: 25619688)
Ecol Lett. 2020 Nov;23(11):1673-1681. (PMID: 32893477)
Nature. 2017 Aug 10;548(7666):210-213. (PMID: 28746307)
Proc Natl Acad Sci U S A. 2023 Jan 17;120(3):e2209043119. (PMID: 36634144)
mSystems. 2019 Feb 5;4(1):. (PMID: 30746494)
Genome Biol. 2016 Jun 03;17(1):121. (PMID: 27259475)
J Allergy Clin Immunol. 2020 Jan;145(1):16-27. (PMID: 31910984)
ISME J. 2020 Jan;14(1):123-134. (PMID: 31578469)
Curr Biol. 2020 Oct 5;30(19):R1189-R1202. (PMID: 33022264)
PLoS Biol. 2021 Feb 19;19(2):e3001116. (PMID: 33606675)
Nature. 2015 Jan 8;517(7533):205-8. (PMID: 25337874)
Cell Host Microbe. 2019 Dec 11;26(6):764-778.e5. (PMID: 31757768)
Front Cell Infect Microbiol. 2022 Mar 04;12:834406. (PMID: 35310856)
J Math Biol. 1989;27(5):537-48. (PMID: 2794803)
Nature. 2017 Dec 14;552(7684):244-247. (PMID: 29211710)
Curr Opin Microbiol. 2014 Apr;18:72-7. (PMID: 24632350)
Nature. 2005 Sep 15;437(7057):356-61. (PMID: 16163346)
ISME J. 2021 Nov;15(11):3119-3128. (PMID: 34127803)
Nat Rev Microbiol. 2010 May;8(5):317-27. (PMID: 20348932)
Cell Microbiol. 2014 Jul;16(7):1024-33. (PMID: 24798552)
Curr Opin Immunol. 2012 Feb;24(1):15-20. (PMID: 22079134)
Front Microbiol. 2015 Apr 23;6:343. (PMID: 25954266)
Environ Microbiol. 2014 Jun;16(6):1472-81. (PMID: 24274586)
Nat Microbiol. 2018 Jan;3(1):47-52. (PMID: 29133883)
Cell Host Microbe. 2020 Feb 12;27(2):199-212.e5. (PMID: 32053789)
ISME J. 2016 Nov;10(11):2557-2568. (PMID: 27022995)
Nature. 2019 Oct;574(7779):549-552. (PMID: 31645729)
معلومات مُعتمدة: R21 AI156817 United States AI NIAID NIH HHS
تواريخ الأحداث: Date Created: 20240422 Date Completed: 20240429 Latest Revision: 20240506
رمز التحديث: 20240506
مُعرف محوري في PubMed: PMC11034675
DOI: 10.1371/journal.pbio.3002346
PMID: 38648198
قاعدة البيانات: MEDLINE
الوصف
تدمد:1545-7885
DOI:10.1371/journal.pbio.3002346