Bacteriophages presence in nature and their role in the natural selection of bacterial populations

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Zakira Naureen
Astrit Dautaj
Kyrylo Anpilogov
Giorgio Camilleri
Kristjana Dhuli
Benedetta Tanzi
Paolo Enrico Maltese
Francesca Cristofoli
Luca De Antoni
Tommaso Beccari
Munis Dundar
Matteo Bertelli


Bacteriophages, spatial/temporal distribution, ecology, microbial communities, natural selection


Phages are the obligate parasite of bacteria and have complex interactions with their hosts. Phages can live in, modify, and shape bacterial communities by bringing about changes in their abundance, diversity, physiology, and virulence. In addition, phages mediate lateral gene transfer, modify host metabolism and reallocate bacterially-derived biochemical compounds through cell lysis, thus playing an important role in ecosystem. Phages coexist and coevolve with bacteria and have developed several antidefense mechanisms in response to bacterial defense strategies against them. Phages owe their existence to their bacterial hosts, therefore they bring about alterations in their host genomes by transferring resistance genes and genes encoding toxins in order to improve the fitness of the hosts. Application of phages in biotechnology, environment, agriculture and medicines demands a deep insight into the myriad of phage-bacteria interactions. However, to understand their complex interactions, we need to know how unique phages are to their bacterial hosts and how they exert a selective pressure on the microbial communities in nature. Consequently, the present review focuses on phage biology with respect to natural selection of bacterial populations.


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1. Lehti TA, Pajunen MI, Skog MS, et al. Internalization of a polysialic acid-binding Escherichia coli bacteriophage into eukaryotic neuroblastoma cells. Nat Commun 2017; 8: 1915
2. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 1998; 281(5374): 237-40.
3. Salmond GP, Fineran PC. A century of the phage: past, present and future. Nat Rev Microbiol 2015; 13(12): 777–86.
4. Svircev A, Roach D, Castle A. Framing the future with bacteriophages in agriculture. Viruses 2018; 10(5).
5. Chan BK, Turner PE, Kim S, Mojibian HR, Elefteriades JA, Narayan D. Phage treatment of an aortic graft infected with Pseudomonas aeruginosa. Evol Med Public Health 2018; 2018(1): 60–6.
6. Ly-Chatain MH. The factors affecting effectiveness of treatment in phages therapy. Front Microbiol 2014; 5: 51.
7. Milo R, Jorgensen P, Moran U, Weber G, Springer M. BioNumbers—the database of key numbers in molecular and cell biology. Nucleic Acids Res 2010; 38: D750–3.
8. Heilmann S, Sneppen K, Krishna S. Sustainability of virulence in a phage-bacterial ecosystem. J Virol 2010; 84(6): 3016–22.
9. Heilmann S, Sneppen K, Krishna S. Coexistence of phage and bacteria on the boundary of self-organized refuges. Proc Natl Acad Sci USA 2012; 109(31): 12828–33.
10. Weitz JS, Hartman H, Levin SA. Coevolutionary arms races between bacteria and bacteriophage. Procee Proc Natl Acad Sci USA 2005; 102(27): 9535–40.
11. Abedon ST. Bacteriophage ecology: Population growth, evolution, and impact of bacterial viruses. Cambridge: Cambridge University Press; 2008.
12. Wright RCT, Friman VP, Smith MCM, Brockhurst MA. Cross-resistance is modular in bacteria-phage interactions. PLoS Biol 2018; 16(10).
13. Gómez P, Buckling A. Bacteria-phage antagonistic coevolution in soil. Science 2011; 332(6025): 106-9.
14. Twort FW. An investigation on the nature of ultra-microscopic viruses. Lancet 1915; 2: 1241–3.
15. d’Herelle F. An invisible microbe that is antagonistic to the dysentery bacillus. Comptes Rendus Academie Sciences Paris 1917; 165: 373–5.
16. Twort FW. The bacteriophage; the breaking down of bacteria by associated filter passing lysins. Br Med J 1922; 2: 293–6.
17. Summers WC. Felix d’Herelle and the origins of molecular biology. New Haven: Yale University Press, 1999.
18. d’Herelle F. Sur l’historique du bacteriophage. Comptes Rendus Sciences Société Biologie Paris 1921; 84: 863–4.
19. d’Herelle F. The nature of bacteriophage. Br Med J 1921; 2: 289–93.
20. Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A. Local adaptation of bacteriophages to their bacterial hosts in soil. Science 2009; 325(5942): 833.
21. Fiers W, Contreras R, Duerinck F, et al. Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature 1976; 260: 500–7.
22. van Regenmortel MH, Mahy BW. Desk encyclopedia of general virology. Academic Press, 2010.
23. Poranen MM, Domanska A in Encyclopedia of Virology (Third Edition), 2008
24. Poranen MM, Mäntynen S, ICTV Report Consortium. ICTV Virus Taxonomy Profile. J Gen Virol 2017; 98: 2423–4.
25. Hong C, Oksanen HM, Liu X, Jakana J, Bamford DH, Chiu W A structural model of the genome packaging process in a membrane-containing double stranded DNA virus. PLoS Biol 2014; 12: e1002024.
26. Murphy FA, Fauquet CM, Bishop DH, et al. Virus taxonomy: classification and nomenclature of viruses. Springer Science & Business Media, 2012.
27. Krupovic M. ICTV virus taxonomy profile: plasmaviridae. J Gen Virol 2018; 99(5): 617-8.
28. Orlova EV. Bacteriophages and their structural organisation. Bacteriophages 2012. doi:10.5772/34642
29. Hyman P, Abedon ST. Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 2010; 70, 217–48.
30. Cenens W, Mebrhatu MT, Makumi A, et al. Expression of a novel P22 ORFan gene reveals the phage carrier state in Salmonella typhimurium. PLoS Genetics 2013; 9: e1003269.
31. Sogin ML, Morrison HG, Huber JA, et al. Microbial diversity in the deep sea and the underexplored “rare biosphere” Proc Natl Acad Sci USA 2006; 103: 12115–20.
32. Atanasova NS, Roine E, Oren A, Bamford DH, Oksanen HM. Global network of specific virus-host interactions in hypersaline environments. Environ Microbiol 2011; 14: 426–40.
33. Reyes A, Wu M, Mcnulty NP, Rohwer FL, Gordon JI. Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. Proc Natl Acad Sci USA 2013; 110: 20236–41.
34. Fancello L, Trape SEB, Robert C, et al. Viruses in the desert: A metagenomic survey of viral communities in four perennial ponds of the Mauritanian Sahara. ISME Journal 2013; 7: 359–69.
35. Koskella B, Thompson JN, Preston GM, Buckling A. Local biotic environment shapes the spatial scale of bacteriophage adaptation to bacteria. Am Nat 2011; 177: 440–51.
36. Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ. The tripartite associations between bacteriophage, wolbachia, and arthropods. PLoS Pathog 2006; 2: e43.
37. Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature 1999; 399: 541–8.
38. Salifu SP, Casey SAC, Foley S. Isolation and characterization of soilborne virulent bacteriophages infecting the pathogen Rhodococcus equi. J Appl Microbiol 2013; 114: 1625–33.
39. Bergh Ø, Børsheim KY, Bratbak G, Heldal M. High abundance of viruses found in aquatic environments. Nature 1989; 340: 467–8.
40. Suttle CA. Viruses in the sea. Nature 2005; 437: 356-61.
41. Weinbauer MG, Peduzzi P. Significance of viruses versus heterotrophic nanofiagellates for controlling bacterial abundance in the northern Adriatic Sea. J Plankton Res 1995; 17: 1851–6.
42. Hennes KP, Simon M. Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake. Appl Environ Microbiol 1995; 61: 333–40.
43. Ashelford KE, Day MJ, Bailey MJ, Lilley AK, Fry JJ. In situ population dynamics of bacterial viruses in a environment. Appl Environ Microbiol 1999; 65: 169-174.
44. Moisa I, Sotropa E, Velehorschi V. Investigation on the presence of cyanophages in fresh and sea waters of Romania. Virologie 1981; 32: 127-32.
45. Ultraphytoplankton in the Central North-Atlantic. Mar Ecol Prog Ser 1995; 122: 1-8.
46. Sullivan MB, Krastins B, Hughes JL, et al. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’. Environ Microbiol 2009; 11: 2935-51.
47. Mann NH, Calendar R. Phages of cyanobacteria. The bacteriophages. Oxford, Oxford University Press, 517–33, 2005.
48. Mühling M, Fuller NJ, Millard A, et al. Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: Evidence for viral control of phytoplankton. Environ Microbiol 2005; 7: 499-508.
49. d'Hérelle F. Le Bactériophage: Son Rôle dans l'Immunité. Paris Masson et cie, 1921.
50. Clokie MR, Millard AD, Letarov AV, Heaphy S. Phages in nature. Bacteriophage 2011; 1(1): 31-45.
51. Cann AJ, Fandrich SE, Heaphy S. Analysis of the virus population present in equine faeces indicates the presence of hundreds of uncharacterized virus genomes. Virus Genes 2005; 30: 151-6.
52. Kulikov EE, Isaeva AS, Rotkina AS, Manykin AA, Letarov AV. Diversity and dynamics of bacteriophages in horse feces. Mikrobiologiia 2007; 76: 271–8.
53. Raoult D, Forterre P. Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008; 4: 315-49.
54. Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc Natl Acad Sci USA 1977; 74(11): 5088-90.
55. Martiny JBH, Bohannan BJM, Brown JH, et al. Microbial biogeography: Putting microorganisms on the map. Nat Rev Microbiol 2006; 4: 102-12.
56. Pietilä MK, Laurinavicius S, Sund J, Roine E, Bamford DH. The single-stranded DNA genome of novel archaeal virus halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J Virol 2010; 84(2): 788-98.
57. Pietilä MK, Roine E, Paulin L, Kalkkinen N, Bamford DH. An ssDNA virus infecting archaea: A new lineage of viruses with a membrane envelope. Mol Microbiol 2009; 72: 307-19.
58. Lawrence CM, Menon S, Eilers BJ, et al. Structural and functional studies of archaeal viruses. J Biol Chem 2009; 12599-603.
59. Happonen LJ, Redder P, Peng X, Reigstad LJ, Prangishvili D, Butcher SJ. Familial relationships in hyperthermo- and acidophilic archaeal viruses. J Virol 2010; 84: 4747-54.
60. Shkoporov AN, Hill C. Bacteriophages of the human gut: The "Known Unknown" of the microbiome. Cell Host Microbe 2019; 25(2): 195-209.
61. Nguyen S, Baker K, Padman BS, et al. Bacteriophage transcytosis provides a mechanism to cross epithelial cell layers. mBio 2017; 8(6): e01874-17.
62. Willner D, Furlan M, Haynes M, et al. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS One 2009; 4(10): e7370.
63. Pride DT, Salzman J, Haynes M, et al. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 2012; 6(5): 915-26.
64. Dethlefsen L, McFall-Ngai M, Relman DA An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 2007; 449(7164): 811-8.
65. Furlan M, Whiteson KL, Erb ML, et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci USA 2013; 110(26): 10771-6.
66. Rodriguez-Brito B, Li L, Wegley L, et al. Viral and microbial community dynamics in four aquatic environments. ISME J 2010; 4(6): 739-51.
67. Gerken TA. Kinetic modeling confirms the biosynthesis of mucin core 1 (beta-Gal(1-3) alpha-GalNAc-O-Ser/Thr) O-glycan structures are modulated by neighboring glycosylation effects. Biochemistry 2004; 43(14): 4137-42.
68. Johansen BK, Wasteson Y, Granum PE, Brynestad S. Mosaic structure of Shiga-toxin-2-encoding phages isolated from Escherichia coli O157:H7 indicates frequent gene exchange between lambdoid phage genomes. Microbiology (Reading) 2001; 147(7): 1929-36.
69. Willner D, Furlan M, Schmieder R, et al. Metagenomic detection of phage-encoded platelet-binding factors in the human oral cavity. Proc Natl Acad Sci USA 2011; 108: 4547-53.
70. Quiberoni A, Suárez VB, Reinheimer JA. Inactivation of Lactobacillus helveticus bacteriophages by thermal and chemical treatments. J Food Prot 1999; 62(8): 894-8.
71. Samson J.E., Moineau S. Bacteriophages in food fermentations: New frontiers in a continuous arms race. Annu Rev Food Sci Technol 2013; 4: 347–68.
72. Dhanashekar R., Akkinepalli S., Nellutla A. Milk-borne infections. An analysis of their potential effect on the milk industry. Germs 2012; 2: 101–9.
73. Emond E, Moineau S. Bacteriophages and food fermentations. In: Bacteriophage: Genetics and Molecular Biology. Horizon Scientific Press/Caister Academic Press, 93-124, 2007.
74. Quiberoni A, Moineau S, Rousseau GM, Reinheimer J, Ackermann H-W. Streptococcus thermophilus bacteriophages. Int Dairy J 2010; 20: 657–64.
75. Karl D, Letelier R, Tupas L, Dore J, Christian J, Hebel D. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 1997; 388(6642): 533–8.
76. Koskella B, Brockhurst MA. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 2014; 38(5): 916-31.
77. Clokie MRJ, Millard AD, Letarov AV, Heaphy S. Phages in nature. Bacteriophage 2011; 1: 31–45.
78. Łos´ M, Wegrzyn G. Pseudolysogeny. Adv Virus Res 2012; 82: 339–49.
79. Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M. Filamentous bacteriophage: Biology, phage display and nanotechnology applications. Curr Issues Mol Biol 2011; 13: 51–76.
80. Pinheiro LAM, Pereira C, Barreal ME, et al. Use of phage ϕ6 to inactivate Pseudomonas syringae pv. actinidiae in kiwifruit plants: in vitro and ex vivo experiments. Appl Microbiol Biotechnol 2020; 104: 1319–30.
81. Siringan P, Connerton PL, Cummings NJ, Connerton IF. Alternative bacteriophage life cycles: The carrier state of Campylobacter jejuni. Open Biol 2014; 4: 130200–1.
82. Bohannan BJ, Lenski RE. Linking genetic change to community evolution: Insights from studies of bacteria and bacteriophage. Ecol Lett 2000; 3: 362–77.
83. Koskella B, Lin DM, Buckling A, Thompson JN. The costs of evolving resistance in heterogeneous parasite environments. Proc R Soc B 2011; 279: 1896–903.
84. Makarova KS, Wolf YI, Koonin EV. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res 2013; 41: 4360–77.
85. van Houte S, Buckling A, Westra ER. Evolutionary ecology of prokaryotic immune mechanisms. Microbiol Mol Biol Rev 2016; 80: 745–63.
86. Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol 2010; 8: 317.
87. Jackson SA, McKenzie RE, Fagerlund RD, Kieper SN, Fineran PC, Brouns SJ. CRISPR-Cas: adapting to change. Science 2017; 356: eaal5056.
88. Levin BR, Moineau S, Bushman M, Barrangou R. The population and evolutionary dynamics of phage and bacteria with CRISPR-mediated immunity. PLoS Genet 2013; 9: e1003312.
89. Seed KD, Lazinski DW, Calderwood SB, Camilli A. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 2013; 494(7438): 489–91.
90. Deveau H, Barrangou R, Garneau JE, et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol 2008; 190: 1390–1400.
91. Semenova E, Jore MM, Datsenko KA, et al. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci USA 2011; 108: 10098–103.
92. Childs LM, Held NL, Young MJ, Whitaker RJ, Weitz JS. Multiscale model of CRISPR-induced coevolutionary dynamics: diversification at the interface of Lamarck and Darwin. Evolution 2012; 66: 2015–29.
93. van Houte S, Ekroth AK, Broniewski JM, et al. The diversity-generating benefits of a prokaryotic adaptive immune system. Nature 2016; 532: 385–8.
94. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 2013; 493: 429.
95. Wittebole X, De Roock S, Opal SM . A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 2014; 5(1): 226-35.
96. Hyman P, Abedon ST. Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 2010; 70: 217–48.
97. Buckling A, Rainey PB. Antagonistic coevolution between a bacterium and a bacteriophage. Proc Biol Sci 2002; 269: 931–6.
98. Scanlan PD, Hall AR, Burlinson P, Preston G, Buckling A. No effect of ksokhost-parasite co-evolution on host range expansion. J Evol Biol 2013; 26: 205–9.
99. Rohwer F, Thurber RV. Viruses manipulate the marine environment. Nature 2009; 459: 207–12.
100. Van Valen L. A new evolutionary law. Evol Theory 1973; 1(1): 1-30.
101. Hall AR, Scanlan PD, Morgan AD, Buckling A. Host-parasite coevolutionary arms races give way to fluctuating selection. Ecol Lett 2011; 14: 635–42.
102. Brockhurst MA, Koskella B. Experimental coevolution of species interactions. Trends Ecol Evol 2013; 28: 367–75.
103. Brockhurst MA, Chapman T, King KC, Mank JE, Paterson S, Hurst GD. Running with the Red Queen: the role of biotic conflicts in evolution. Proc Biol Sci 2014; 281(1797): 20141382.
104. Rodriguez-Brito B, Li LL, Wegley L, et al. Viral and microbial community dynamics in four aquatic environments. Isme J 2010; 4: 739–51.
105. Breitbart M, Rohwer F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol 2005; 13(6): 278–84.
106. Fuhrman JA, Noble RT. Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 1995; 40: 1236-42.
107. Bikard D, Marraffini LA. Innate and adaptive immunity in bacteria: Mechanisms of programmed genetic variation to fight bacteriophages. Curr Opin Immunol 2012; 24(1): 15-20.
108. Parsons RJ, Breitbart M, Lomas MW, Carlson CA. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J 2012; 6: 273–84.
109. Cochran PK, Paul JH. Seasonal abundance of lysogenic bacteria in a subtropical estuary. Appl Environ Microbiol 1998; 64: 2308–12.
110. Goh S, Hussain H, Chang BJ, Emmett W, Riley TV, Mullany P. PhageC2 mediates transduction of Tn6215, encoding erythromycin resistance, between Clostridium difficile strains. mBio 2013; 4: e00840-13.
111. Evans TJ, Crow MA, Williamson NR, et al. Characterization of a broad-host-range flagellum dependent phage that mediates high-efficiency generalized transduction in, and between, Serratia and Pantoea. Microbiology 2009; 156: 240–7.
112. Marti E, Variatza E, Balcázar JL. Bacteriophages as a reservoir of extended-spectrum β-lactamase and fluoroquinolone resistance genes in the environment. Clin Microbiol Infect 2014; 20(7): O456-9.
113. Scott AE, Timms AR, Connerton PL, Loc Carrillo C, Adzfa Radzum K, Connerton IF. Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathogens 2007; 3: e119.
114. Clokie MRJ, Shan J, Bailey S, et al. Transcription of a “photosynthetic” T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 2006; 8: 827–35.
115. Wang X, Kim Y, Ma Q, et al. Cryptic prophages help bacteria cope with adverse environments. Nat Commun 2010; 1: 147.
116. Wagner PL, Waldor MK. Bacteriophage control of bacterial virulence. Infect Immun 2002; 70: 3985–93.
117. Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996; 272: 1910–4.
118. Hayashi T, Baba T, Matsumoto H, Terawaki Y. Phage-conversion of cytotoxin production in Pseudomonas aeruginosa. Mol Microbiol 1990; 4: 1703–9.
119. McDonough MA, Butterton JR. Spontaneous tandem amplification and deletion of the shiga toxin operon in Shigella dysenteriae 1. Mol Microbiol 1999; 34: 1058–69.
120. Poulton EB. Notes upon, or suggested by, the colours, markings, and protective attitudes of certain lepidopterous larvae and pupae, and of a phytophagous hymenopterous larva. Transactions of the Royal Entomological Society of London 1884; 27–60.
121. Rice SA, Tan CH, Mikkelsen PJ, et al. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J 2008; 3: 271–82.
122. Cenens W, Mebrhatu MT, Makumi A, et al. Expression of a novel P22 ORFan gene reveals the phage carrier state in Salmonella typhimurium. PLoS Genet 2013; 9: e1003269.
123. Ram ASP, Boucher D, Sime Ngando T, Debroas D, Romagoux JC. Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: Coupling with temperature. Microb Ecol 2005; 50: 64–72.
124. Haerter J, Mitarai N, Sneppen K. Phage and bacteria support mutual diversity in a narrowing staircase of coexistence. ISME J 2014; 8: 2317–26.
125. Brown SP, Le Chat L, De Paepe M, Taddei F. Ecology of microbial invasions: Amplification allows virus carriers to invade more rapidly when rare. Curr Biol 2006; 16: 2048–52.
126. Cordero OX, Polz MF. Explaining microbial genomic diversity in light of evolutionary ecology. Nat Rev Microbiol 2014; 12: 263–73.
127. Thingstad TF. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 2000; 45: 1320–8.
128. Vage S, Storesund JE, Thingstad TF. Adding a cost of resistance description extends the ability of virus-host model to explain observed patterns in structure and function of pelagic microbial communities. Environ Microbiol 2013; 15: 1842–52.
129. Campbell BJ, Yu L, Heidelberg JF, Kirchman DL. Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci USA 2011; 108: 12776–81.
130. Cryan JF, Dinan TG. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13(10): 701–12.
131. Łusiak-Szelachowska M, Weber-Dąbrowska B, Jończyk-Matysiak E, Wojciechowska R, Górski A. Bacteriophages in the gastrointestinal tract and their implications. Gut Pathog 2017; 9: 44.
132. Peduzzi P, Gruber M, Gruber M, Schagerl M. The virus’s tooth: cyanophages affect an African flamingo population in a bottom-up cascade. ISME J 2014; 8: 1346–51.
133. Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 2009; 325: 992–4.
134. Suttle CA. Marine viruses—Major players in the global ecosystem. Nat Rev Microbiol 2007; 5: 801–12.
135. Wilhelm SW, Suttle CA. Viruses and nutrient cycles in the sea. BioScience 1999; 49: 781–8.
136. Lennon JT, Martiny JBH. Rapid evolution buffers ecosystem impacts of viruses in a microbial food web. Ecol Lett 2008; 11: 1178–88.
137. Suttle CA, Chan AM, Cottrell MT. Infection of phytoplankton by viruses and reduction of primary productivity. Nature 1990; 347: 467–9.
138. Käse L, Geuer JK. Phytoplankton responses to marine climate change – An Introduction. In: YOUMARES 8 – Oceans Across Boundaries: Learning from each other. Springer, Cham, 2018.

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