Lysogeny destabilizes computationally simulated microbiomes.


Journal

Ecology letters
ISSN: 1461-0248
Titre abrégé: Ecol Lett
Pays: England
ID NLM: 101121949

Informations de publication

Date de publication:
Jun 2024
Historique:
revised: 06 05 2024
received: 03 01 2024
accepted: 06 06 2024
medline: 26 6 2024
pubmed: 26 6 2024
entrez: 26 6 2024
Statut: ppublish

Résumé

Microbiomes are ecosystems, and their stability can impact the health of their hosts. Theory predicts that predators influence ecosystem stability. Phages are key predators of bacteria in microbiomes, but phages are unusual predators because many have lysogenic life cycles. It has been hypothesized that lysogeny can destabilize microbiomes, but lysogeny has no direct analog in classical ecological theory, and no formal theory exists. We studied the stability of computationally simulated microbiomes with different numbers of temperate (lysogenic) and virulent (obligate lytic) phage species. Bacterial populations were more likely to fluctuate over time when there were more temperate phages species. After disturbances, bacterial populations returned to their pre-disturbance densities more slowly when there were more temperate phage species, but cycles engendered by disturbances dampened more slowly when there were more virulent phage species. Our work offers the first formal theory linking lysogeny to microbiome stability.

Identifiants

pubmed: 38923281
doi: 10.1111/ele.14464
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14464

Subventions

Organisme : Horizon 2020 Framework Programme
ID : 767015
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/T008725/1
Pays : United Kingdom

Informations de copyright

© 2024 The Author(s). Ecology Letters published by John Wiley & Sons Ltd.

Références

Ahmed, H.I., Herrera, M., Liew, Y.J. & Aranda, M. (2019) Long‐term temperature stress in the coral model Aiptasia supports the “Anna Karenina Principle” for bacterial microbiomes. Frontiers in Microbiology, 10, 975.
Allesina, S. & Tang, S. (2012) Stability criteria for complex ecosystems. Nature, 483, 205–208.
Bao, H.‐D., Pang, M.‐D., Olaniran, A., Zhang, X.‐H., Zhang, H., Zhou, Y. et al. (2018) Alterations in the diversity and composition of mice gut microbiota by lytic or temperate gut phage treatment. Applied Microbiology and Biotechnology, 102, 10219–10230.
Brives, C. & Pourraz, J. (2020) Phage therapy as a potential solution in the fight against AMR: obstacles and possible futures. Palgrave Communications, 6, 1–11.
Brown, C.M., Lawrence, J.E. & Campbell, D.A. (2006) Are phytoplankton population density maxima predictable through analysis of host and viral genomic DNA content? Journal of the Marine Biological Association of the United Kingdom, 86, 491–498.
Castillo, D., Kauffman, K., Hussain, F., Kalatzis, P., Rørbo, N., Polz, M.F. et al. (2018) Widespread distribution of prophage‐encoded virulence factors in marine Vibrio communities. Scientific Reports, 8, 9973.
Caswell, H. (1978) Predator‐mediated coexistence: a nonequilibrium model. The American Naturalist, 112, 127–154.
Chan, B.K., Abedon, S.T. & Loc‐Carrillo, C. (2013) Phage cocktails and the future of phage therapy. Future Microbiology, 8, 769–783.
Cohen, Y., Pollock, F.J., Rosenberg, E. & Bourne, D.G. (2013) Phage therapy treatment of the coral pathogen Vibrio coralliilyticus. MIcrobiologyOpen, 2, 64–74.
Cortes, M.G., Krog, J. & Balázsi, G. (2019) Optimality of the spontaneous prophage induction rate. Journal of Theoretical Biology, 483, 110005.
Coyte, K.Z., Schluter, J. & Foster, K.R. (2015) The ecology of the microbiome: networks, competition, and stability. Science, 350, 663–666.
Czyz, A., Los, M., Wrobel, B. & Wegrzyn, G. (2001) Inhibition of spontaneous induction of lambdoid prophages in Escherichia coli cultures: simple procedures with possible biotechnological applications. BMC Biotechnology, 1, 1.
Dadgostar, P. (2019) Antimicrobial resistance: implications and costs. Infection and Drug Resistance, 12, 3903–3910.
Dahlman, S., Avellaneda‐Franco, L. & Barr, J.J. (2021) Phages to shape the gut microbiota? Current Opinion in Biotechnology, 68, 89–95.
Davies, E.V., Winstanley, C., Fothergill, J.L. & James, C.E. (2016) The role of temperate bacteriophages in bacterial infection. Microbiology Letters, 363, fnw015.
Diamond, J.M. (2005) Guns, germs, and steel: the fates of human societies. New York: Norton.
Doak, D.F., Bigger, D., Harding, E.K., Marvier, M.A., O'Malley, R.E. & Thomson, D. (1998) The statistical inevitability of stability–diversity relationships in community ecology. The American Naturalist, 151, 264–276.
Edlin, G., Lin, L.E.O. & Kudrna, R. (1975) λ lysogens of E. coli reproduce more rapidly than non‐lysogens. Nature, 255, 735–737.
Elton, C. (1927) Animal ecology. New York: The Macmillan Company.
Fillol‐Salom, A., Alsaadi, A., de Sousa, J.A.M., Zhong, L., Foster, K.R., Rocha, E.P.C. et al. (2019) Bacteriophages benefit from generalized transduction. PLoS Pathogens, 15, e1007888.
Ford, S., Moeskjær, S., Young, P., Santamaria, R.I. & Harrison, E. (2021) Introducing a novel, broad host range temperate phage family infecting Rhizobium leguminosarum and beyond. Frontiers in Microbiology, 12, 765271.
Fortuna, M.A., Barbour, M.A., Zaman, L., Hall, A.R., Buckling, A. & Bascompte, J. (2019) Coevolutionary dynamics shape the structure of bacteria‐phage infection networks. Evolution, 73, 1001–1011.
Galla, T. (2018) Dynamically evolved community size and stability of random Lotka‐Volterra ecosystems. Europhysics Letters, 123, 48004.
Gandon, S. (2016) Why be temperate: lessons from bacteriophage λ. Trends in Microbiology, 24, 356–365.
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. (1996) Local adaptation and gene‐for‐gene coevolution in a metapopulation model. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263, 1003–1009.
Gurney, J., Aldakak, L., Betts, A., Gougat‐Barbera, C., Poisot, T., Kaltz, O. et al. (2017) Network structure and local adaptation in co‐evolving bacteria‐phage interactions. Molecular Ecology, 26, 1764–1777.
Gutierrez, B. & Domingo‐Calap, P. (2020) Phage therapy in gastrointestinal diseases. Microorganisms, 8, 1420.
Hargreaves, K.R., Clokie, M. & Kropinski, A. (2014) Bacteriophage behavioural ecology: how phages alter their bacterial host's habits. Bacteriophage, 4, e29866.
Holmes, I., Harris, K. & Quince, C. (2012) Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One, 7, e30126.
Howard‐Varona, C., Hargreaves, K.R., Abedon, S.T. & Sullivan, M.B. (2017) Lysogeny in nature: mechanisms, impact and ecology of temperate phages. The ISME Journal, 11, 1511–1520.
Ives, A.R. & Carpenter, S.R. (2007) Stability and diversity of ecosystems. Science, 317, 58–62.
Kaul, D., Rathnasinghe, R., Ferres, M., Tan, G.A., Barrera, A., Pickett, B.E. et al. (2020) Microbiome disturbance and resilience dynamics of the upper respiratory tract during influenza a virus infection. Nature Communications, 11, 2537.
Keddy, P.A. & Shipley, B. (1989) Competitive hierarchies in herbaceous plant communities. Oikos, 54, 234–241.
Kim, M.‐S. & Bae, J.‐W. (2018) Lysogeny is prevalent and widely distributed in the murine gut microbiota. The ISME Journal, 12, 127–1141.
Knowles, B., Bonachela, J.A., Behrenfeld, M.J., Bondoc, K.G., Cael, B.B., Carlson, C.A. et al. (2020) Temperate infection in a virus–host system previously known for virulent dynamics. Nature Communications, 11, 4626.
Koskella, B. & Brockhurst, M.A. (2014) Bacteria‐phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiology Reviews, 38, 916–931.
Koskella, B., Hernandez, C.A. & Wheatley, R.M. (2022) Understanding the impacts of bacteriophage viruses: from laboratory evolution to natural ecosystems. Annual Review of Virology, 9, 57–78.
Koskella, B. & Meaden, S. (2013) Understanding bacteriophage specificity in natural microbial communities. Viruses, 5, 806–823.
Kourilsky, P. (1973) Lysogenization by bacteriophage lambda: 1. Multiple infection and lysogenic response. Molecular and General Genetics, 122, 183–195.
Larsson, D.G.J. & Flach, C.F. (2022) Antibiotic resistance in the environment. Nature Reviews. Microbiology, 20, 257–269.
Leggett, H.C., Buckling, A., Long, G.H. & Boots, M. (2013) Generalism and the evolution of parasite virulence. Trends in Ecology & Evolution, 28, 592–596.
Li, X.Y., Lachnit, T., Fraune, S., Bosch, T.C.G., Traulsen, A. & Sieber, M. (2017) Temperate phages as self‐replicating weapons in bacterial competition. Journal of the Royal Society Interface, 14, 20170563.
Lin, L., Bitner, R. & Edlin, G. (1977) Increased reproductive fitness of Escherichia coli lambda lysogens. Journal of Virology, 21, 554–559.
Lin, Y., Berger, U., Grimm, V. & Qian‐Ru, J. (2012) Differences between symmetric and asymmetric facilitation matter: exploring the interplay between modes of positive and negative plant interactions. Journal of Ecology, 100, 1482–1491.
Loreau, M., Barbier, M., Filotas, E., Gravel, D., Isbell, F., Miller, S.J. et al. (2021) Biodiversity as insurance: from concept to measurement and application. Biological Reviews of the Cambridge Philosophical Society, 96, 2333–2354.
Loreau, M. & de Mazancourt, C. (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecology Letters, 16(Suppl 1), 106–115.
Luque, A. & Sileira, C.B. (2020) Quantification of lysogeny caused by phage coinfections in microbial communities from biophysical principles. mSystems, 5, e00353‐20.
MacArthur, R. (1955) Fluctuations of animal populations, and a measure of community stability. Ecology, 36, 533–536.
May, R.M. (1973) Stability and complexity in model ecosystems. Princeton, NJ: Princeton University Press.
Melechen, N.E. & Go, G. (1980) Induction of lambdoid prophages by amino acid deprivation: differential inducibility; role of recA. Molecular & General Genetics, 180, 147–155.
Mills, S., Shanahan, F., Stanton, C., Hill, C., Coffey, A. & Ross, R.P. (2013) Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes, 4, 4–16.
Mougi, A. & Kondoh, M. (2012) Diversity of interaction types and ecological community stability. Science, 337, 349–351.
Ni, J., Wu, G.D., Albenberg, L. & Tomov, V.T. (2017) Gut microbiota and IBD: causation or correlation? Nature Reviews. Gastroenterology & Hepatology, 14, 573–584.
Paine, R.T. (1966) Food web complexity and species diversity. The American Naturalist, 100, 65–75.
Pargin, E., Roach, M.J., Skye, A., Papudeshi, B., Inglis, L.K., Mallawaarachchi, V. et al. (2023) The human gut virome: composition, colonization, interactions, and impacts on human health. Frontiers in Microbiology, 14, 963173.
Paul, J.H. (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? The ISME Journal, 2, 579–589.
Peixoto, R.S., Sweet, M., Villela, H.D.M., Cardoso, P., Thomas, T., Voolstra, C.R. et al. (2021) Coral probiotics: premise, promise, prospects. Annual Review of Animal Biosciences, 9, 265–288.
Pimm, S.L. (1991) The balance of nature? Ecological issues in the conservation of species and communities. Chicago & London: University of Chicago Press.
Poullain, V., Gandon, S., Brockhurst, M.A., Buckling, A. & Hochberg, M.E. (2008) The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution, 62, 1–11.
Shreiner, A.B., Kao, J.Y. & Young, V.B. (2015) The gut microbiome in health and in disease. Current Opinion in Gastroenterology, 31, 69–75.
Silpe, J.E., Duddy, O.P. & Bassler, B.L. (2023) Induction mechanisms and strategies underlying interprophage competition during polylysogeny. PLoS Pathogens, 19, e1011363.
Suh, G.A., Lodise, T.P., Tamma, P.D., Knisely, J.M., Alexander, J., Aslam, S. et al. (2022) Considerations for the use of phage therapy in clinical practice. Antimicrobial Agents and Chemotherapy, 66, e0207121.
Sutton, T.D.S. & Hill, C. (2019) Gut bacteriophage: current understanding and challenges. Frontiers in Endocrinology, 10, 784.
Sweere, J.M., van Belleghem, J.D., Ishak, H., Bach, M.S., Popescu, M., Sunkari, V. et al. (2019) Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science, 363, eaat9691.
Tang, W.H., Kitai, T. & Hazen, S.L. (2017) Gut microbiota in cardiovascular health and disease. Circulation Research, 120, 1183–1196.
Thingstad, F.T. (1997) A theoretical approach to structuring mechanisms in the pelagic food web. Hydrobiologia, 363, 59–72.
Thingstad, T.F. (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnology and Oceanography, 45, 1320–1328.
Thingstad, T.F. & Lignell, R. (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology, 13, 19–27.
Thingstad, T.F., Vage, S., Storesund, J.E., Sandaa, R.A. & Giske, J. (2014) A theoretical analysis of how strain‐specific viruses can control microbial species diversity. Proceedings of the National Academy of Sciences of the United States of America, 111, 7813–7818.
Tolstoy, L. (2015) Anna Karenina. Minneapolis, MN: Lerner Publishing Group, Inc.
Townsend, E.M., Kelly, L., Muscatt, G., Box, J.D., Hargraves, N., Lilley, D. et al. (2021) The human gut phageome: origins and roles in the human gut microbiome. Frontiers in Cellular and Infection Microbiology, 11, 643214.
Uyttebroek, S., Chen, B., Onsea, J., Ruythooren, F., Debaveye, Y., Devolder, D. et al. (2022) Safety and efficacy of phage therapy in difficult‐to‐treat infections: a systematic review. The Lancet Infectious Diseases, 22, e208–e220.
Voigt, R.M., Forsyth, C.B., Green, S.J. & Engen, P.A. (2016) Circadian rhythm and the gut microbiome. International Review of Neurobiology, 131, 193–205.
Weitz, J.S. (2016) Quantitative viral ecology: dynamics of viruses and their microbial hosts. Princeton, NJ: Princeton University Press.
Zaneveld, J.R., McMinds, R. & Vega Thurber, R. (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nature Microbiology, 2, 17121.
Zioutis, C., Seki, D., Bauchinger, F., Herbold, C., Berger, A., Wisgrill, L. et al. (2022) Ecological processes shaping microbiomes of extremely low birthweight infants. Frontiers in Microbiology, 13, 812136.
Zu, J., Wang, W., Takeuchi, Y., Zu, B. & Wang, K. (2008) On evolution under symmetric and asymmetric competitions. Journal of Theoretical Biology, 254, 239–251.
Zuppi, M., Hendrickson, H.L., O'Sullivan, J.M. & Vatanen, T. (2021) Phages in the gut ecosystem. Frontiers in Cellular and Infection Microbiology, 11, 822562.

Auteurs

R Tucker Gilman (RT)

Department of Earth and Environmental Sciences, Faculty of Science and Engineering, University of Manchester, Manchester, UK.

Mark R Muldoon (MR)

Department of Mathematics, Faculty of Science and Engineering, University of Manchester, Manchester, UK.

Spyridon Megremis (S)

Division of Infection, Immunity and Respiratory Medicine, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.
Department of Genetics and Genome Biology, Centre for Phage Research, Institute for Precision Health, University of Leicester, Leicester, UK.

David L Robertson (DL)

MRC-University of Glasgow Centre for Virus Research, Glasgow, UK.

Nina Chanishvili (N)

George Eliava Institute of Bacteriophages, Microbiology and Virology, Tbilisi, Georgia.
Ivane Javakhishvili Tbilisi State University, Tbilisi, Georgia.
NewVision University, Tbilisi, Georgia.

Nikolaos G Papadopoulos (NG)

Allergy Department, 2nd Pediatric Clinic, University of Athens, Athens, Greece.
Lydia Becker Institute of Immunology and Inflammation, University of Manchester, Manchester, UK.

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