{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,21]],"date-time":"2026-04-21T03:37:42Z","timestamp":1776742662787,"version":"3.51.2"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010400","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,8,18]],"date-time":"2022-08-18T00:00:00Z","timestamp":1660780800000}}],"reference-count":39,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2022,8,8]],"date-time":"2022-08-08T00:00:00Z","timestamp":1659916800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["740704"],"award-info":[{"award-number":["740704"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009708","name":"Novo Nordisk Fonden","doi-asserted-by":"publisher","award":["NNF21OC0068775"],"award-info":[{"award-number":["NNF21OC0068775"]}],"id":[{"id":"10.13039\/501100009708","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Phages and bacteria manage to coexist and sustain ecosystems with a high diversity of strains, despite limited resources and heavy predation. This diversity can be explained by the \u201ckill the winner\u201d model where virulent phages predominantly prey on fast-growing bacteria and thereby suppress the competitive exclusion of slower-growing bacteria. Here we computationally investigate the robustness of these systems against invasions, where new phages or bacteria may interact with more than one of the resident strains. The resulting interaction networks were found to self-organize into a network with strongly interacting specialized predator-prey pairs, resembling that of the \u201ckill the winner\u201d model. Furthermore, the \u201ckill the winner\u201d dynamics is enforced with the occasional elimination of even the fastest-growing bacteria strains due to a phage infecting the fast and slow growers. The frequency of slower-growing strains was increased with the introduction of even a few non-diagonal interactions. Hence, phages capable of infecting multiple hosts play significant roles both in the evolution of the ecosystem by eliminating the winner and in supporting diversity by allowing slow growers to coexist with faster growers.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010400","type":"journal-article","created":{"date-parts":[[2022,8,8]],"date-time":"2022-08-08T17:34:51Z","timestamp":1659980091000},"page":"e1010400","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":44,"title":["From kill the winner to eliminate the winner in open phage-bacteria systems"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5831-8578","authenticated-orcid":true,"given":"Anastasios","family":"Marantos","sequence":"first","affiliation":[]},{"given":"Namiko","family":"Mitarai","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9820-3567","authenticated-orcid":true,"given":"Kim","family":"Sneppen","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,8,8]]},"reference":[{"key":"pcbi.1010400.ref001","first-page":"6","volume-title":"A century of phage research: bacteriophages and the shaping of modern biology","author":"EC Keen","year":"2015"},{"key":"pcbi.1010400.ref002","doi-asserted-by":"crossref","unstructured":"Moebus K, Nattkemper H. 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Volterra","year":"1926","journal-title":"Memoria della regia accademia nazionale del lincei ser"},{"issue":"16\/17","key":"pcbi.1010400.ref013","first-page":"461","article-title":"The growth of mixed populations: Two species competing for a common food supply","volume":"22","author":"AJ Lotka","year":"1932","journal-title":"Journal of the Washington Academy of Sciences"},{"key":"pcbi.1010400.ref014","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1097\/00010694-193602000-00018","article-title":"The Struggle for Existence","volume":"41","author":"GF Gause","year":"1936","journal-title":"Soil Science"},{"key":"pcbi.1010400.ref015","doi-asserted-by":"crossref","first-page":"1292","DOI":"10.1126\/science.131.3409.1292","article-title":"The competitive exclusion principle","volume":"131","author":"G Hardin","year":"1960","journal-title":"Science"},{"key":"pcbi.1010400.ref016","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1086\/282676","article-title":"Community Equilibria and Stability, and an Extension of the Competitive Exclusion Principle","volume":"104","author":"SA Levin","year":"1970","journal-title":"The American Naturalist"},{"key":"pcbi.1010400.ref017","doi-asserted-by":"crossref","DOI":"10.5962\/bhl.title.27468","volume-title":"The Genetical Theory Of Natural Selection","author":"RA Fisher","year":"1930"},{"key":"pcbi.1010400.ref018","doi-asserted-by":"crossref","first-page":"2317","DOI":"10.1038\/ismej.2014.80","article-title":"Phage and bacteria support mutual diversity in a narrowing staircase of coexistence","volume":"8.11","author":"JO Haerter","year":"2014","journal-title":"ISME Journal"},{"key":"pcbi.1010400.ref019","doi-asserted-by":"crossref","first-page":"7813","DOI":"10.1073\/pnas.1400909111","article-title":"A theoretical analysis of how strain-specific viruses can control microbial species diversity","volume":"111.21","author":"TF Thingstad","year":"2014","journal-title":"Proceedings of the National Academy of 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the Panglossian paradigm: a critique of the adaptationist programme. 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Biological Sciences"},{"key":"pcbi.1010400.ref024","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1111\/ele.12912","article-title":"Network spandrels reflect ecological assembly","volume":"21.3","author":"DS Maynard","year":"2018","journal-title":"Ecology letters"},{"key":"pcbi.1010400.ref025","doi-asserted-by":"crossref","first-page":"268101","DOI":"10.1103\/PhysRevLett.119.268101","article-title":"Coevolution maintains diversity in the stochastic \u201cKill the Winner\u201d model","volume":"119.26","author":"C Xue","year":"2017","journal-title":"Physical review letters"},{"key":"pcbi.1010400.ref026","volume-title":"Elements of Physical Biology","author":"AJ Lotka","year":"1925"},{"key":"pcbi.1010400.ref027","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1111\/j.1558-5646.1961.tb03139.x","article-title":"Conditions for the Existence of Bacteriophage","volume":"15","author":"A Campbell","year":"1961","journal-title":"Evolution"},{"key":"pcbi.1010400.ref028","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.4319\/lo.1995.40.7.1236","article-title":"Viruses and protists cause similar bacterial mortality in coastal seawater","volume":"40.7","author":"JA Fuhrman","year":"1995","journal-title":"Limnology and oceanography"},{"key":"pcbi.1010400.ref029","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1128\/aem.63.1.77-83.1997","article-title":"Virus decay and its causes in coastal waters","volume":"63.1","author":"RT Noble","year":"1997","journal-title":"Applied and Environmental Microbiology"},{"key":"pcbi.1010400.ref030","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1086\/283134","article-title":"Resource-Limited Growth, Competition, and Predation: A Model and Experimental Studies with Bacteria and Bacteriophage","volume":"111","author":"BR Levin","year":"1977","journal-title":"The American Naturalist"},{"key":"pcbi.1010400.ref031","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1128\/mBio.00126-12","article-title":"Spatial structure and Lamarckian adaptation explain extreme genetic diversity at CRISPR Locus","volume":"3","author":"JO Haerter","year":"2012","journal-title":"mBio"},{"key":"pcbi.1010400.ref032","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1007\/BF01983456","article-title":"Taxonomic investigations of bacteriophage sensitive bacteria isolated from marine waters","volume":"36.4","author":"K Moebus","year":"1983","journal-title":"Helgolander Meeresuntersuchungen"},{"key":"pcbi.1010400.ref033","doi-asserted-by":"crossref","first-page":"4128","DOI":"10.1128\/AEM.64.11.4128-4133.1998","article-title":"Bacteriophage Diversity in the North Sea","volume":"64","author":"A Wichels","year":"1998","journal-title":"Applied and environmental microbiology"},{"key":"pcbi.1010400.ref034","doi-asserted-by":"crossref","first-page":"6730","DOI":"10.1128\/AEM.01399-07","article-title":"Large Variabilities in Host Strain Susceptibility and Phage Host Range Govern Interactions between Lytic Marine Phages and Their Flavobacterium Hosts","volume":"73.21","author":"K Holmfeldt","year":"2007","journal-title":"Applied and Environmental Microbiology"},{"key":"pcbi.1010400.ref035","doi-asserted-by":"crossref","first-page":"2048","DOI":"10.1016\/j.cub.2006.08.089","article-title":"Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare","volume":"16.20","author":"SP Brown","year":"2006","journal-title":"Current Biology"},{"key":"pcbi.1010400.ref036","first-page":"221","article-title":"Evolutionary response of predator to dangerous prey-reduction of toxicity of newts and resistance of garter snakes in island populations","volume":"45.1","author":"ED Brodie","year":"1991","journal-title":"Evolution"},{"key":"pcbi.1010400.ref037","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1046\/j.1523-1739.1997.96368.x","article-title":"Insular endemic plants lack defenses against herbivores","volume":"11.5","author":"L Bowen","year":"1997","journal-title":"Conservation Biology"},{"key":"pcbi.1010400.ref038","doi-asserted-by":"crossref","first-page":"20130033","DOI":"10.1098\/rsfs.2013.0033","article-title":"Coevolutionary diversification creates nested-modular structure in phage\u2013bacteria interaction networks","volume":"3.6","author":"SJ Beckett","year":"2013","journal-title":"Interface focus"},{"key":"pcbi.1010400.ref039","doi-asserted-by":"crossref","first-page":"e1004440","DOI":"10.1371\/journal.pcbi.1004440","article-title":"Diversity waves in collapse-driven population dynamics","volume":"11.9","author":"S Maslov","year":"2015","journal-title":"PLoS computational 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