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Abstract

Viruses of bacteria (bacteriophages or phage) have broad effects on bacterial ecology and evolution in nature that mediate microbial interactions, shape bacterial diversity, and influence nutrient cycling and ecosystem function. The unrelenting impact of phages within the microbial realm is the result, in large part, of their ability to rapidly evolve in response to bacterial host dynamics. The knowledge gained from laboratory systems, typically using pairwise interactions between single-host and single-phage systems, has made clear that phages coevolve with their bacterial hosts rapidly, somewhat predictably, and primarily by counteradapting to host resistance. Recent advancement in metagenomics approaches, as well as a shifting focus toward natural microbial communities and host-associated microbiomes, is beginning to uncover the full picture of phage evolution and ecology within more complex settings. As these data reach their full potential, it will be critical to ask when and how insights gained from studies of phage evolution in vitro can be meaningfully applied to understanding bacteria-phage interactions in nature. In this review, we explore the myriad ways that phagesshape and are themselves shaped by bacterial host populations and communities, with a particular focus on observed and predicted differences between the laboratory and complex microbial communities.

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2022-09-29
2024-12-13
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Literature Cited

  1. 1.
    Dennehy JJ. 2009. Bacteriophages as model organisms for virus emergence research. Trends Microbiol 17:450–57
    [Crossref] [Google Scholar]
  2. 2.
    Breitbart M, Bonnain C, Malki K, Sawaya NA. 2018. Phage puppet masters of the marine microbial realm. Nat. Microbiol. 3:754–66
    [Crossref] [Google Scholar]
  3. 3.
    Chevallereau A, Pons BJ, van Houte S, Westra ER. 2022. Interactions between bacterial and phage communities in natural environments. Nat. Rev. Microbiol. 20:49–62
    [Crossref] [Google Scholar]
  4. 4.
    Scanlan PD. 2017. Bacteria–bacteriophage coevolution in the human gut: implications for microbial diversity and functionality. Trends Microbiol 25:8614–23
    [Crossref] [Google Scholar]
  5. 5.
    De Sordi L, Lourenço M, Debarbieux L. 2019. The battle within: interactions of bacteriophages and bacteria in the gastrointestinal tract. Cell Host Microbe 25:210–18
    [Crossref] [Google Scholar]
  6. 6.
    Twort FW. 1915. An investigation on the nature of ultramicroscopic viruses. Lancet 186:48141241–43
    [Crossref] [Google Scholar]
  7. 7.
    d'Herelle F. 1917. Sur un microbe invisible antagoniste des bacilles dysentériques. C. R. Acad. Sci. 165:373–75
    [Google Scholar]
  8. 8.
    Buckling A, Maclean RC, Brockhurst MA, Colegrave N. 2009. The Beagle in a bottle. Nature 457:824–29
    [Crossref] [Google Scholar]
  9. 9.
    Piligrimova EG, Kazantseva OA, Kazantsev AN, Nikulin NA, Skorynina AV et al. 2021. Putative plasmid prophages of Bacillus cereus sensu lato may hold the key to undiscovered phage diversity. Sci. Rep. 11:7611
    [Crossref] [Google Scholar]
  10. 10.
    Hampton HG, Watson BN, Fineran PC. 2020. The arms race between bacteria and their phage foes. Nature 577:327–36
    [Crossref] [Google Scholar]
  11. 11.
    Mutalik VK, Adler BA, Rishi HS, Piya D, Zhong C et al. 2020. High-throughput mapping of the phage resistance landscape in E. coli. PLOS Biol 18:10e3000877
    [Crossref] [Google Scholar]
  12. 12.
    Kortright KE, Chan BK, Turner PE. 2020. High-throughput discovery of phage receptors using transposon insertion sequencing of bacteria. PNAS 117:3118670–79
    [Crossref] [Google Scholar]
  13. 13.
    Samson JE, Magadán AH, Sabri M, Moineau S. 2013. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11:10675–87
    [Crossref] [Google Scholar]
  14. 14.
    Yehl K, Lemire S, Yang AC, Ando H, Mimee M et al. 2019. Engineering phage host-range and suppressing bacterial resistance through phage tail fiber mutagenesis. Cell 179:2459–69
    [Crossref] [Google Scholar]
  15. 15.
    Leinweber H, Sieber RN, Larsen J, Stegger M, Ingmer H. 2021. Staphylococcal phages adapt to new hosts by extensive attachment site variability. mBio 12:6e02259–21
    [Crossref] [Google Scholar]
  16. 16.
    Bohannan BJ, Lenski RE. 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3:362–77
    [Crossref] [Google Scholar]
  17. 17.
    Kerr B, Neuhauser C, Bohannan BJ, Dean AM. 2006. Local migration promotes competitive restraint in a host–pathogen ‘tragedy of the commons. .’ Nature 442:75–78
    [Crossref] [Google Scholar]
  18. 18.
    Lopez Pascua L, Hall AR, Best A, Morgan AD, Boots M et al. 2014. Higher resources decrease fluctuating selection during host–parasite coevolution. Ecol. Lett. 17:111380–88
    [Crossref] [Google Scholar]
  19. 19.
    Betts A, Kaltz O, Hochberg ME. 2014. Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages. PNAS 111:11109–14
    [Crossref] [Google Scholar]
  20. 20.
    Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C et al. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. . J. Bacteriol. 190:1390–400
    [Crossref] [Google Scholar]
  21. 21.
    van Houte S, Ekroth AK, Broniewski JM, Chabas H, Ashby B et al. 2016. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 532:7599385–88
    [Crossref] [Google Scholar]
  22. 22.
    Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER et al. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. PNAS 108:2510098–103
    [Crossref] [Google Scholar]
  23. 23.
    Paez-Espino D, Sharon I, Morovic W, Stahl B, Thomas BC et al. 2015. CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. mBio 6:2ez00262–15
    [Crossref] [Google Scholar]
  24. 24.
    Koskella B. 2013. Phage-mediated selection on microbiota of a long-lived host. Curr. Biol. 23:131256–60
    [Crossref] [Google Scholar]
  25. 25.
    Dewald-Wang EA, Parr N, Tiley K, Lee A, Koskella B. 2022. Multiyear time-shift study of bacteria and phage dynamics in the phyllosphere. Am. Nat. 199:126–40
    [Crossref] [Google Scholar]
  26. 26.
    Laanto E, Hoikkala V, Ravantti J, Sundberg LR. 2017. Long-term genomic coevolution of host-parasite interaction in the natural environment. Nat. Commun. 8:1111
    [Crossref] [Google Scholar]
  27. 27.
    Guerrero LD, Pérez MV, Orellana E, Piuri M, Quiroga C et al. 2021. Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system. ISME J 15:636–48
    [Crossref] [Google Scholar]
  28. 28.
    Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD et al. 2013. Rapid evolution of the human gut virome. PNAS 110:3012450–55
    [Crossref] [Google Scholar]
  29. 29.
    Koskella B, Meaden S. 2013. Understanding bacteriophage specificity in natural microbial communities. Viruses 5:3806–23
    [Crossref] [Google Scholar]
  30. 30.
    de Jonge PA, Nobrega FL, Brouns SJ, Dutilh BE. 2019. Molecular and evolutionary determinants of bacteriophage host range. Trends Microbiol 27:51–63
    [Crossref] [Google Scholar]
  31. 31.
    Koskella B, Thompson JN, Preston GM, Buckling A. 2011. Local biotic environment shapes the spatial scale of bacteriophage adaptation to bacteria. Am. Nat. 177:4440–51
    [Crossref] [Google Scholar]
  32. 32.
    Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A. 2009. Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325:5942833
    [Crossref] [Google Scholar]
  33. 33.
    Van Cauwenberghe J, Santamaría RI, Bustos P, Juárez S, Ducci MA et al. 2021. Spatial patterns in phage-Rhizobium coevolutionary interactions across regions of common bean domestication. ISME J 15:72092–106
    [Crossref] [Google Scholar]
  34. 34.
    Roux S, Hawley AK, Beltran MT, Scofield M, Schwientek P et al. 2014. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. eLife 3:e03125
    [Crossref] [Google Scholar]
  35. 35.
    Džunková M, Low SJ, Daly JN, Deng L, Rinke C et al. 2019. Defining the human gut host–phage network through single-cell viral tagging. Nat. Microbiol. 4:2192–203
    [Crossref] [Google Scholar]
  36. 36.
    Berg M, Goudeau D, Olmsted C, McMahon KD, Yitbarek S et al. 2021. Host population diversity as a driver of viral infection cycle in wild populations of green sulfur bacteria with long standing virus-host interactions. ISME J 15:1569–84
    [Crossref] [Google Scholar]
  37. 37.
    Marbouty M, Thierry A, Millot GA, Koszul R 2021. MetaHiC phage-bacteria infection network reveals active cycling phages of the healthy human gut. eLife 10:e60608
    [Crossref] [Google Scholar]
  38. 38.
    Gunathilaka GU, Tahlan V, Mafiz AI, Polur M, Zhang Y. 2017. Phages in urban wastewater have the potential to disseminate antibiotic resistance. Int. J. Antimicrob. Agents 50:678–83
    [Crossref] [Google Scholar]
  39. 39.
    Göller PC, Elsener T, Lorgé D, Radulovic N, Bernardi V et al. 2021. Multi-species host range of staphylococcal phages isolated from wastewater. Nat. Comm. 12:6965
    [Crossref] [Google Scholar]
  40. 40.
    Wheatley RM, MacLean RC. 2021. CRISPR-Cas systems restrict horizontal gene transfer in Pseudomonas aeruginosa. ISME J 15:51420–33
    [Crossref] [Google Scholar]
  41. 41.
    Hall AR, Scanlan PD, Morgan AD, Buckling A. 2011. Host–parasite coevolutionary arms races give way to fluctuating selection. Ecol. Lett. 14:635–42
    [Crossref] [Google Scholar]
  42. 42.
    Schwartz DA, Lindell D. 2017. Genetic hurdles limit the arms race between Prochlorococcus and the T7-like podoviruses infecting them. ISME J 11:81836–51
    [Crossref] [Google Scholar]
  43. 43.
    Shapiro JW, Turner PE. 2018. Evolution of mutualism from parasitism in experimental virus populations. Evolution 72:3707–12
    [Crossref] [Google Scholar]
  44. 44.
    Thingstad TF, Lignell R. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13:119–27
    [Crossref] [Google Scholar]
  45. 45.
    Harcombe WR, Bull JJ. 2005. Impact of phages on two-species bacterial communities. . Appl. Environ. Microbiol. 71:5254–59
    [Crossref] [Google Scholar]
  46. 46.
    Bettarel Y, Sime-Ngando T, Amblard C, Dolan J. 2004. Viral activity in two contrasting lake ecosystems. Appl. Environ. Microb. 70:2941–51
    [Crossref] [Google Scholar]
  47. 47.
    Poisot T, Bell T, Martinez E, Gougat-Barbera C, Hochberg ME. 2013. Terminal investment induced by a bacteriophage in a rhizosphere bacterium. F1000Research 1:21
    [Crossref] [Google Scholar]
  48. 48.
    Pourtois J, Tarnita CE, Bonachela JA. 2020. Impact of lytic phages on phosphorus- vs. nitrogen-limited marine microbes. Front. Microbiol. 11:221
    [Crossref] [Google Scholar]
  49. 49.
    Lynch M, Marinov GK. 2015. The bioenergetic costs of a gene. PNAS 112:5115690–95
    [Crossref] [Google Scholar]
  50. 50.
    Kirchberger PC, Martinez ZA, Luker LJ, Ochman H. 2021. Defensive hypervariable regions confer superinfection exclusion in microviruses. PNAS 118:28e2102786118
    [Crossref] [Google Scholar]
  51. 51.
    Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS et al. 2016. Prophages mediate defense against phage infection through diverse mechanisms. ISME J. 10:2854–66
    [Crossref] [Google Scholar]
  52. 52.
    Kondo K, Kawano M, Sugai M 2021. Distribution of antimicrobial resistance and virulence genes within the prophage-associated regions in nosocomial pathogens. mSphere 6:4e00452–21
    [Crossref] [Google Scholar]
  53. 53.
    Hernandez CA, Koskella B. 2019. Phage resistance evolution in vitro is not reflective of in vivo outcome in a plant-bacteria-phage system. Evolution 73:2461–75
    [Crossref] [Google Scholar]
  54. 54.
    Meaden S, Paszkiewicz K, Koskella B. 2015. The cost of phage resistance in a plant pathogenic bacterium is context-dependent. Evolution 69:51321–28
    [Crossref] [Google Scholar]
  55. 55.
    Wimmer F, Beisel CL. 2020. CRISPR-Cas systems and the paradox of self-targeting spacers. Front. Microbiol. 10:3078
    [Crossref] [Google Scholar]
  56. 56.
    Markwitz P, Lood C, Olszak T, van Noort V, Lavigne R, Drulis-Kawa Z. 2022. Genome-driven elucidation of phage-host interplay and impact of phage resistance evolution on bacterial fitness. ISME J 16:2533–42
    [Crossref] [Google Scholar]
  57. 57.
    Meaden S, Capria L, Alseth E, Gandon S, Biswas A et al. 2021. Phage gene expression and host responses lead to infection-dependent costs of CRISPR immunity. ISME J 15:2534–44
    [Crossref] [Google Scholar]
  58. 58.
    Bohannan BJ, Kerr B, Jessup CM, Hughes JB, Sandvik G. 2002. Trade-offs and coexistence in microbial microcosms. Antonie Van Leeuwenhoek 81:107–15
    [Crossref] [Google Scholar]
  59. 59.
    Avrani S, Schwartz DA, Lindell D. 2012. Virus-host swinging party in the oceans: incorporating biological complexity into paradigms of antagonistic coexistence. Mob. Genet. Elem. 2:88–95
    [Crossref] [Google Scholar]
  60. 60.
    Chaudhry WN, Pleška M, Shah NN, Weiss H, McCall IC et al. 2018. Leaky resistance and the conditions for the existence of lytic bacteriophage. PLOS Biol 16:e2005971
    [Crossref] [Google Scholar]
  61. 61.
    Skanata A, Kussell E. 2021. Ecological memory preserves phage resistance mechanisms in bacteria. Nat. Commun. 12:6817
    [Crossref] [Google Scholar]
  62. 62.
    Levin BR, Bull JJ. 2004. Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2:2166–73
    [Crossref] [Google Scholar]
  63. 63.
    Wright RCT, Friman V-P, Smith MCM, Brockhurst MA. 2019. Resistance evolution against phage combinations depends on the timing and order of exposure. mBio 10:5e01652–19
    [Crossref] [Google Scholar]
  64. 64.
    Zhang Q-G, Chu X-L, Buckling A. 2021. Overcoming the growth–infectivity trade-off in a bacteriophage slows bacterial resistance evolution. Evol. Appl. 14:82055–63
    [Crossref] [Google Scholar]
  65. 65.
    Arbas SM, Narayanasamy S, Herold M, Lebrun LA, Hoopmann MR et al. 2021. Roles of bacteriophages, plasmids and CRISPR immunity in microbial community dynamics revealed using time-series integrated meta-omics. Nat. Microbiol. 6:123–35
    [Crossref] [Google Scholar]
  66. 66.
    Tétart F, Desplats C, Kutateladze M, Monod C, Ackermann HW, Krisch HM. 2001. Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages. J. Bacteriol. 183:1358–66
    [Crossref] [Google Scholar]
  67. 67.
    Pratama AA, Chaib De Mares M, Van Elsas JD 2018. Evolutionary history of bacteriophages in the genus Paraburkholderia. Front. Microbiol. 9:835
    [Crossref] [Google Scholar]
  68. 68.
    Kupczok A, Neve H, Huang KD, Hoeppner MP, Heller KJ et al. 2018. Rates of mutation and recombination in Siphoviridae phage genome evolution over three decades. Mol. Biol. Evol. 35:51147–59
    [Crossref] [Google Scholar]
  69. 69.
    Dion MB, Oechslin F, Moineau S. 2020. Phage diversity, genomics and phylogeny. Nat. Rev. Microbiol. 18:125–38
    [Crossref] [Google Scholar]
  70. 70.
    Mavrich TN, Hatfull GF. 2017. Bacteriophage evolution differs by host, lifestyle and genome. Nat. Microbiol. 2:917112
    [Crossref] [Google Scholar]
  71. 71.
    Levin BR, Bull JJ. 1996. Phage therapy revisited: the population biology of a bacterial infection and its treatment with bacteriophage and antibiotics. Am. Nat. 147:6881–98
    [Crossref] [Google Scholar]
  72. 72.
    Bull JJ, Christensen KA, Scott C, Jack BR, Crandall CJ et al. 2018. Phage-bacterial dynamics with spatial structure: Self organization around phage sinks can promote increased cell densities. Antibiotics 7:8
    [Crossref] [Google Scholar]
  73. 73.
    Lourenço M, Chaffringeon L, Lamy-Besnier Q, Pedron T, Campagne P et al. 2020. The spatial heterogeneity of the gut limits predation and fosters coexistence of bacteria and bacteriophages. Cell Host Microbe 28:3390–401
    [Crossref] [Google Scholar]
  74. 74.
    Scanlan PD. 2020. Resistance may be futile: Gut spatial heterogeneity supports bacteria-phage co-existence. Cell Host Microbe 28:3356–58
    [Crossref] [Google Scholar]
  75. 75.
    Eriksen RS, Mitarai N, Sneppen K. 2020. Sustainability of spatially distributed bacteria-phage systems. Sci. Rep. 10:3154
    [Crossref] [Google Scholar]
  76. 76.
    Pires DP, Melo LD, Azeredo J. 2021. Understanding the complex phage-host interactions in biofilm communities. Annu. Rev. Virol. 8:73–94
    [Crossref] [Google Scholar]
  77. 77.
    Testa S, Berger S, Piccardi P, Oechslin F, Resch G, Mitri S. 2019. Spatial structure affects phage efficacy in infecting dual-strain biofilms of Pseudomonas aeruginosa. Commun. Biol. 2:1405
    [Crossref] [Google Scholar]
  78. 78.
    Simmons EL, Bond MC, Koskella B, Drescher K, Bucci V, Nadell CD. 2020. Biofilm structure promotes coexistence of phage-resistant and phage-susceptible bacteria. mSystems 5:3e00877–19
    [Crossref] [Google Scholar]
  79. 79.
    Pyenson NC, Marraffini LA 2020. Co-evolution within structured bacterial communities results in multiple expansion of CRISPR loci and enhanced immunity. eLife 9:e53078
    [Crossref] [Google Scholar]
  80. 80.
    Berngruber TW, Lion S, Gandon S 2013. Evolution of suicide as a defence strategy against pathogens in a spatially structured environment. Ecol. Lett. 16:446–53
    [Crossref] [Google Scholar]
  81. 81.
    Attrill EL, Claydon R, Łapińska U, Recker M, Meaden S et al. 2021. Individual bacteria in structured environments rely on phenotypic resistance to phage. PLOS Biol 19:e3001406
    [Crossref] [Google Scholar]
  82. 82.
    Abedon ST, Culler RR 2007. Bacteriophage evolution given spatial constraint. J. Theor. Biol. 248:111–19
    [Crossref] [Google Scholar]
  83. 83.
    Berngruber TW, Lion S, Gandon S 2015. Spatial structure, transmission modes and the evolution of viral exploitation strategies. PLOS Pathog. 11:e1004810
    [Crossref] [Google Scholar]
  84. 84.
    Vogwill T, Fenton A, Brockhurst MA. 2010. How does spatial dispersal network affect the evolution of parasite local adaptation?. Evolution 64:61795–801
    [Crossref] [Google Scholar]
  85. 85.
    You X, Kallies R, Kühn I, Schmidt M, Harms H et al. 2021. Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system. ISME J https://doi.org/10.1038/s41396-021-01155-x
    [Crossref] [Google Scholar]
  86. 86.
    Velásquez AC, Huguet-Tapia JC, He SY. 2021. Phyllosphere-inhabiting endophytic bacteria feature a stationary phase-like lifestyle. bioRxiv 2021.05.10.443510. https://doi.org/10.1101/2021.05.10.443510
    [Crossref]
  87. 87.
    Shachrai I, Zaslaver A, Alon U, Dekel E. 2010. Cost of unneeded proteins in E. coli is reduced after several generations in exponential growth. Mol. Cell 38:5758–67
    [Crossref] [Google Scholar]
  88. 88.
    Kivisaar M. 2003. Stationary phase mutagenesis: mechanisms that accelerate adaptation of microbial populations under environmental stress. Environ. Microbiol. 5:10814–27
    [Crossref] [Google Scholar]
  89. 89.
    Finkel SE. 2006. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat. Rev. Microbiol. 4:113–20
    [Crossref] [Google Scholar]
  90. 90.
    Krueger AP, Fong J. 1937. The relationship between bacterial growth and phage production. J. Gen. Physiol. 21:2137–50
    [Crossref] [Google Scholar]
  91. 91.
    Bryan D, El-Shibiny A, Hobbs Z, Porter J, Kutter EM. 2016. Bacteriophage T4 infection of stationary phase E. coli: life after log from a phage perspective. Front. Microbiol. 7:1391
    [Crossref] [Google Scholar]
  92. 92.
    Chenoweth MR, Somerville GA, Krause DC, O'Reilly KL, Gherardini FC 2004. Growth characteristics of Bartonella henselae in a novel liquid medium: primary isolation, growth-phase-dependent phage induction, and metabolic studies. Appl. Environ. Microbiol. 70:656–63
    [Crossref] [Google Scholar]
  93. 93.
    Liang X, Zhang Y, Wommack KE, Wilhelm SW, DeBruyn JM et al. 2020. Lysogenic reproductive strategies of viral communities vary with soil depth and are correlated with bacterial diversity. Soil Biol. Biochem. 144:107767
    [Crossref] [Google Scholar]
  94. 94.
    Weld RJ, Butts C, Heinemann JA. 2004. Models of phage growth and their applicability to phage therapy. J. Theor. Biol. 227:11–11
    [Crossref] [Google Scholar]
  95. 95.
    Maurice CF, Bouvier T, Comte J, Guillemette F, Del Giorgio PA 2010. Seasonal variations of phage life strategies and bacterial physiological states in three northern temperate lakes. Environ. Microbiol. 12:3628–41
    [Crossref] [Google Scholar]
  96. 96.
    Egilmez HI, Morozov AY, Galyov EE. 2021. Modelling the spatiotemporal complexity of interactions between pathogenic bacteria and a phage with a temperature-dependent life cycle switch. Sci. Rep. 11:4382
    [Crossref] [Google Scholar]
  97. 97.
    Abdulrahman AR, Suttle CA, Agustí S 2021. Moderate seasonal dynamics indicate an important role for lysogeny in the Red Sea. Microorganisms 9:1269
    [Crossref] [Google Scholar]
  98. 98.
    Hevroni G, Philosof A 2021. Daily and seasonal rhythms of marine phages of cyanobacteria. Circadian Rhythms in Bacteria and Microbiomes CH Johnson, MJ Rust 387–415 Cham, Switz: Springer
    [Google Scholar]
  99. 99.
    Gallet R, Lenormand T, Wang IN. 2012. Phenotypic stochasticity protects lytic bacteriophage populations from extinction during the bacterial stationary phase. Evolution 66:3485–94
    [Crossref] [Google Scholar]
  100. 100.
    Petrie KL, Palmer ND, Johnson DT, Medina SJ, Yan SJ et al. 2018. Destabilizing mutations encode nongenetic variation that drives evolutionary innovation. Science 359:63831542–45
    [Crossref] [Google Scholar]
  101. 101.
    Bohannan BJ, Lenski RE. 1997. Effect of resource enrichment on a chemostat community of bacteria and bacteriophage. Ecology 78:2303–15
    [Crossref] [Google Scholar]
  102. 102.
    Harrison E, Laine AL, Hietala M, Brockhurst MA. 2013. Rapidly fluctuating environments constrain coevolutionary arms races by impeding selective sweeps. Proc. R. Soc. B 280:20130937
    [Crossref] [Google Scholar]
  103. 103.
    Zhang X, Xiong D, Yu J, Yang H, He P, Wei H. 2021. Genetic polymorphism drives susceptibility between bacteria and bacteriophages. Front. Microbiol. 12:627897
    [Crossref] [Google Scholar]
  104. 104.
    Chevallereau A, Meaden S, van Houte S, Westra ER, Rollie C. 2019. The effect of bacterial mutation rate on the evolution of CRISPR-Cas adaptive immunity. Philos. Trans. R. Soc. B 374:20180094
    [Crossref] [Google Scholar]
  105. 105.
    Scanlan JG, Hall AR, Scanlan PD. 2019. Impact of bile salts on coevolutionary dynamics between the gut bacterium Escherichia coli and its lytic phage PP01. Infect. Genet. Evol. 73:425–32
    [Crossref] [Google Scholar]
  106. 106.
    Vogwill T, Fenton A, Buckling A, Hochberg ME, Brockhurst MA. 2009. Source populations act as coevolutionary pacemakers in experimental selection mosaics containing hotspots and coldspots. Am. Nat. 173:5E171–76
    [Crossref] [Google Scholar]
  107. 107.
    Sieber M, Robb M, Forde SE, Gudelj I. 2014. Dispersal network structure and infection mechanism shape diversity in a coevolutionary bacteria-phage system. ISME J 8:3504–14
    [Crossref] [Google Scholar]
  108. 108.
    Morgan AD, Gandon S, Buckling A. 2005. The effect of migration on local adaptation in a coevolving host–parasite system. Nature 437:7056253–56
    [Crossref] [Google Scholar]
  109. 109.
    England WE, Kim T, Whitaker RJ. 2018. Metapopulation structure of CRISPR-Cas immunity in Pseudomonas aeruginosa and its viruses. mSystems 3:e00075–18
    [Crossref] [Google Scholar]
  110. 110.
    Kunin V, He S, Warnecke F, Peterson SB, Martin HG et al. 2008. A bacterial metapopulation adapts locally to phage predation despite global dispersal. Genome Res 18:2293–97
    [Crossref] [Google Scholar]
  111. 111.
    Darch SE, Kragh KN, Abbott EA, Bjarnsholt T, Bull JJ et al. 2017. Phage inhibit pathogen dissemination by targeting bacterial migrants in a chronic infection model. mBio 8:e00240–17
    [Google Scholar]
  112. 112.
    Yu Z, Schwarz C, Zhu L, Chen L, Shen Y, Yu P 2020. Hitchhiking behavior in bacteriophages facilitates phage infection and enhances carrier bacteria colonization. Environ. Sci. Technol. 55:42462–72
    [Crossref] [Google Scholar]
  113. 113.
    Pope WH, Bowman CA, Russell DA, Jacobs-Sera D, Asai DJ et al. 2015. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. eLife 4:e06416
    [Crossref] [Google Scholar]
  114. 114.
    Flores CO, Meyer JR, Valverde S, Farr L, Weitz JS. 2011. Statistical structure of host–phage interactions. PNAS 108:E288–97
    [Crossref] [Google Scholar]
  115. 115.
    Lee S, Sieradzki ET, Nicolas AM, Walker RL, Firestone MK et al. 2021. Methane-derived carbon flows into host–virus networks at different trophic levels in soil. PNAS 118:32e2105124118
    [Crossref] [Google Scholar]
  116. 116.
    Refardt D. 2011. Within-host competition determines reproductive success of temperate bacteriophages. ISME J 5:91451–60
    [Crossref] [Google Scholar]
  117. 117.
    Kauffman KM, Chang WK, Brown JM, Hussain FA, Yang JY et al. 2022. Resolving the structure of phage–bacteria interactions in the context of natural diversity. Nat. Commun. 13:1372
    [Crossref] [Google Scholar]
  118. 118.
    Koskella B, Lin DM, Buckling A, Thompson JN. 2012. The costs of evolving resistance in heterogeneous parasite environments. Proc. R. Soc. B 279:17351896–903
    [Crossref] [Google Scholar]
  119. 119.
    Betts A, Gray C, Zelek M, MacLean RC, King KC. 2018. High parasite diversity accelerates host adaptation and diversification. Science 360:907–11
    [Crossref] [Google Scholar]
  120. 120.
    Broniewski JM, Meaden S, Paterson S, Buckling A, Westra ER. 2020. The effect of phage genetic diversity on bacterial resistance evolution. ISME J 14:828–36
    [Crossref] [Google Scholar]
  121. 121.
    Meaden S, Biswas A, Arkhipova K, Morales SE, Dutilh BE et al. 2021. High viral abundance and low diversity are associated with increased CRISPR-Cas prevalence across microbial ecosystems. Curr. Biol. 32:220–27.e5
    [Crossref] [Google Scholar]
  122. 122.
    Blazanin M, Turner PE. 2021. Community context matters for bacteria-phage ecology and evolution. ISME J 15:3119–28
    [Crossref] [Google Scholar]
  123. 123.
    Sant DG, Woods LC, Barr JJ, McDonald MJ. 2021. Host diversity slows bacteriophage adaptation by selecting generalists over specialists. Nat. Ecol. Evol. 5:3350–59
    [Crossref] [Google Scholar]
  124. 124.
    Hussain FA, Dubert J, Elsherbini J, Murphy M, Vaninsberghe D et al. 2021. Rapid evolutionary turnover of mobile genetic elements drives bacterial resistance to phages. Science 374:488–92
    [Crossref] [Google Scholar]
  125. 125.
    Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML et al. 2013. Bacteriophage adhering to mucus provide a non–host-derived immunity. PNAS 110:10771–76
    [Crossref] [Google Scholar]
  126. 126.
    Johnke J, Baron M, de Leeuw M, Kushmaro A, Jurkevitch E et al. 2017. A generalist protist predator enables coexistence in multitrophic predator-prey systems containing a phage and the bacterial predator Bdellovibrio. Front. Ecol. Evol. 5:124
    [Crossref] [Google Scholar]
  127. 127.
    Brown JM, Labonté JM, Brown J, Record NR, Poulton NJ et al. 2020. Single cell genomics reveals viruses consumed by marine protists. Front. Microbiol. 11:2317
    [Crossref] [Google Scholar]
  128. 128.
    Wilhelm SW, Suttle CA. 1999. Viruses and nutrient cycles in the sea: Viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49:10781–88
    [Crossref] [Google Scholar]
  129. 129.
    Ghanem N, Stanley CE, Harms H, Chatzinotas A, Wick LY. 2019. Mycelial effects on phage retention during transport in a microfluidic platform. Environ. Sci. Technol. 53:11755–63
    [Crossref] [Google Scholar]
  130. 130.
    Penner JC, Ferreira JA, Secor PR, Sweere JM, Birukova MK et al. 2016. Pf4 bacteriophage produced by Pseudomonas aeruginosa inhibits Aspergillus fumigatus metabolism via iron sequestration. Microbiology 162:91583–94
    [Crossref] [Google Scholar]
  131. 131.
    Friman V-P, Buckling A. 2013. Effects of predation on real-time host–parasite coevolutionary dynamics. Ecol. Lett. 16:39–46
    [Crossref] [Google Scholar]
  132. 132.
    Örmälä-Odegrip AM, Ojala V, Hiltunen T, Zhang J, Bamford JK et al. 2015. Protist predation can select for bacteria with lowered susceptibility to infection by lytic phages. BMC Evol. Biol. 15:181
    [Crossref] [Google Scholar]
  133. 133.
    terHorst CP, Zee PC, Heath KD, Miller TE, Pastore AI et al. 2018. Evolution in a community context: trait responses to multiple species interactions. Am. Nat. 191:3368–80
    [Crossref] [Google Scholar]
  134. 134.
    McClean D, Friman VP, Finn A, Salzberg LI, Donohue I. 2019. Coping with multiple enemies: Pairwise interactions do not predict evolutionary change in complex multitrophic communities. Oikos 128:111588–99
    [Crossref] [Google Scholar]
  135. 135.
    Arnold JW, Koudelka GB. 2014. The Trojan Horse of the microbiological arms race: phage-encoded toxins as a defence against eukaryotic predators. Environ. Microbiol. 16:454–66
    [Crossref] [Google Scholar]
  136. 136.
    Green SI, Gu Liu C, Yu X, Gibson S, Salmen W et al. 2021. Targeting of mammalian glycans enhances phage predation in the gastrointestinal tract. mBio 12:e03474–20
    [Crossref] [Google Scholar]
  137. 137.
    Roach DR, Leung CY, Henry M, Morello E, Singh D et al. 2017. Synergy between the host immune system and bacteriophage is essential for successful phage therapy against an acute respiratory pathogen. Cell Host Microbe 22:138–47
    [Crossref] [Google Scholar]
  138. 138.
    Bull JJ, Gill JJ. 2014. The habits of highly effective phages: population dynamics as a framework for identifying therapeutic phages. Front. Microbiol. 5:618
    [Crossref] [Google Scholar]
  139. 139.
    Nguyen S, Baker K, Padman BS, Patwa R, Dunstan RA et al. 2017. Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio 8:6e01874–17
    [Crossref] [Google Scholar]
  140. 140.
    Van Belleghem JD, Dąbrowska K, Vaneechoutte M, Barr JJ, Bollyky PL. 2019. Interactions between bacteriophage, bacteria, and the mammalian immune system. Viruses 11:110
    [Crossref] [Google Scholar]
  141. 141.
    Bichet MC, Chin WH, Richards W, Lin YW, Avellaneda-Franco L et al. 2021. Bacteriophage uptake by mammalian cell layers represents a potential sink that may impact phage therapy. iScience 24:102287
    [Crossref] [Google Scholar]
  142. 142.
    Lindberg HM, McKean KA, Wang IN 2014. Phage fitness may help predict phage therapy efficacy. Bacteriophage 4:4e964081
    [Crossref] [Google Scholar]
  143. 143.
    Gelman D, Yerushalmy O, Alkalay-Oren S, Rakov C, Ben-Porat S et al. 2021. Clinical phage microbiology: a suggested framework and recommendations for the in-vitro matching steps of phage therapy. Lancet Microbe 2:e555–63
    [Crossref] [Google Scholar]
  144. 144.
    Castledine M, Padfield D, Sierocinski P, Pascual JS, Hughes A et al. 2021. Parallel evolution of phage resistance-virulence trade-offs during in vitro and nasal Pseudomonas aeruginosa phage treatment. bioRxiv 2021.09.06.459069. https://doi.org/10.1101/2021.09.06.459069
    [Crossref]
  145. 145.
    Chan BK, Sistrom M, Wertz JE, Kortright KE, Narayan D, Turner PE. 2016. Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci. Rep. 6:26717
    [Crossref] [Google Scholar]
  146. 146.
    Gordillo Altamirano F, Forsyth JH, Patwa R, Kostoulias X, Trim M et al. 2021. Bacteriophage-resistant Acinetobacter baumannii are resensitized to antimicrobials. Nat. Microbiol. 6:157–61
    [Crossref] [Google Scholar]
  147. 147.
    Gurney J, Pradier L, Griffin JS, Gougat-Barbera C, Chan BK et al. 2020. Phage steering of antibiotic-resistance evolution in the bacterial pathogen, Pseudomonas aeruginosa. Evol. Med. Public Health 2020:1148–57
    [Crossref] [Google Scholar]
  148. 148.
    Lourenço M, De Sordi L, Debarbieux L. 2018. The diversity of bacterial lifestyles hampers bacteriophage tenacity. Viruses 10:6327
    [Crossref] [Google Scholar]
  149. 149.
    Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A et al. 2017. Communication between viruses guides lysis–lysogeny decisions. Nature 541:488–93
    [Crossref] [Google Scholar]
  150. 150.
    Sweere JM, Van Belleghem JD, Ishak H, Bach MS, Popescu M et al. 2019. Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science 363:6434eaat9691
    [Crossref] [Google Scholar]
  151. 151.
    Popescu M, Van Belleghem JD, Khosravi A, Bollyky PL. 2021. Bacteriophages and the immune system. Annu. Rev. Virol. 8:415–35
    [Crossref] [Google Scholar]
  152. 152.
    Morella NM, Gomez AL, Wang G, Leung MS, Koskella B. 2018. The impact of bacteriophages on phyllosphere bacterial abundance and composition. Mol. Ecol. 27:82025–38
    [Crossref] [Google Scholar]
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