pp 1-38 | Cite as

Population Genomics of Bacteriophages

Part of the Population Genomics book series


Due to their small genome size, an abundance equaling or surpassing that of bacteria, and an obligatory dependence on their host bacteria, bacteriophages are an ideal study object for population genomics. However, due to a certain research neglect, less than 2,700 phage genomes were deposited in the NCBI database, far less than the 90,000 prokaryotic genomes. Large and ecologically representative phage genome sequencing projects have so far only conducted for a small number of phage systems. Phages of dairy bacteria belong to this group since they were systematically collected and extensively sequenced due to their negative impact on industrial milk fermentation. More than ten different phage species were defined for Lactococcus lactis and four for Streptococcus thermophilus, the two most important starter bacteria in cheese and yogurt production, respectively. The genetic interrelationship between the phages infecting the same host species and between phages infecting phylogenetically (L. lactis vs. L. garvieae and S. thermophilus vs. S. salivarius phages) or ecologically closely related host bacteria (L. lactis vs. S. thermophilus dairy phages) is here reviewed. Dairy phages allowed the study of population genomics as a function of time, geography, and distinct fermentation technologies. The elucidation of the CRISPR-Cas antiviral defense system in S. thermophilus provided first insights into the phage-bacterium arms race at the level of phage and bacterial population genomics. Phages studied by applied microbiologists thus became important study objects for fundamental questions of biology.


Bacteriophages Cheese Dairy Lactic acid bacteria Lactococcus Milk fermentation Phylogeny Population genomics Streptococcus Taxonomy 



The author thanks Douwe van Sinderen (University College Cork, Ireland) and Shawna McCallin (University of Lausanne, Switzerland) for their critical reading of the manuscript and many useful comments.


  1. Achigar R, Magadán AH, Tremblay DM, Julia Pianzzola M, Moineau S. Phage-host interactions in Streptococcus thermophilus: genome analysis of phages isolated in Uruguay and ectopic spacer acquisition in CRISPR array. Sci Rep. 2017;7:43438.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  2. Ackermann HW. Bacteriophage observations and evolution. Res Microbiol. 2003;154(4):245–51.PubMedCrossRefGoogle Scholar
  3. Ackermann HW. Classification of bacteriophages. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 8–16.Google Scholar
  4. Ackermann HW, Kropinski AM. Curated list of prokaryote viruses with fully sequenced genomes. Res Microbiol. 2007;158(7):555–66.PubMedCrossRefGoogle Scholar
  5. Ackermann HW, DuBow MS, Jarvis AW, Jones LA, Krylov VN, Maniloff J, Rocourt J, Safferman RS, Schneider J, Seldin L. The species concept and its application to tailed phages. Arch Virol. 1992;124(1–2):69–82.PubMedCrossRefGoogle Scholar
  6. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315(5819):1709–12.ADSPubMedCrossRefGoogle Scholar
  7. Binetti AG, Del Río B, Martín MC, Alvarez MA. Detection and characterization of Streptococcus thermophilus bacteriophages by use of the antireceptor gene sequence. Appl Environ Microbiol. 2005;71(10):6096–103.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Blatny JM, Godager L, Lunde M, Nes IF. Complete genome sequence of the Lactococcus lactis temperate phage phiLC3: comparative analysis of phiLC3 and its relatives in lactococci and streptococci. Virology. 2004;318(1):231–44.Google Scholar
  9. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology. 2005;151(Pt 8):2551–61.PubMedGoogle Scholar
  10. Botstein D. A theory of modular evolution for bacteriophages. Ann N Y Acad Sci. 1980;354:484–90.ADSPubMedCrossRefGoogle Scholar
  11. Bouchard JD, Moineau S. Homologous recombination between a lactococcal bacteriophage and the chromosome of its host strain. Virology. 2000;270(1):65–75.Google Scholar
  12. Bourdin G, Navarro A, Sarker SA, Pittet AC, Qadri F, Sultana S, Cravioto A, Talukder KA, Reuteler G, Brüssow H. Coverage of diarrhoea-associated Escherichia coli isolates from different origins with two types of phage cocktails. Microb Biotechnol. 2014;7(2):165–76.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Braun V, Hertwig S, Neve H, Geis A, Teuber M. Taxonomic differentiation of bacteriophages of Lactococcus lactis by electron microscopy, DNA-DNA hybridization, and protein profiles. J Gen Microbial. 1989;135:2551–60.Google Scholar
  14. Brüssow H. Phages of dairy bacteria. Annu Rev Microbiol. 2001;55:283–303.PubMedCrossRefGoogle Scholar
  15. Brüssow H. The impact of phages on the evolution of bacterial pathogenicity. In: Pallen M, Nelson KE, Preston GM, editors. Bacterial pathogenomics. Washington: ASM Press; 2007. p. 267–300.CrossRefGoogle Scholar
  16. Brüssow H. Phage-bacterium co-evolution and its implication for bacterial pathogenesis. In: Hensel M, Schmidt H, editors. Horizontal gene transfer in the evolution of pathogenesis. New York: Cambridge University Press; 2008. p. 49–77.CrossRefGoogle Scholar
  17. Brüssow H. The not so universal tree of life or the place of viruses in the living world. Philos Trans R Soc Lond Ser B Biol Sci. 2009;364(1527):2263–74.CrossRefGoogle Scholar
  18. Brüssow H, Bruttin A. Characterization of a temperate Streptococcus thermophilus bacteriophage and its genetic relationship with lytic phages. Virology. 1995;212(2):632–40.PubMedCrossRefGoogle Scholar
  19. Brüssow H, Desiere F. Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol Microbiol. 2001;39(2):213–22.PubMedCrossRefGoogle Scholar
  20. Brüssow H, Desiere F. Evolution of tailed phages: insights from comparative phage genomics. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 26–36.Google Scholar
  21. Brüssow H, Hendrix RW. Phage genomics: small is beautiful. Cell. 2002;108(1):13–6.PubMedCrossRefGoogle Scholar
  22. Brüssow H, Fremont M, Bruttin A, Sidoti J, Constable A, Fryder V. Detection and classification of Streptococcus thermophilus bacteriophages isolated from industrial milk fermentation. Appl Environ Microbiol. 1994a;60(12):4537–43.PubMedPubMedCentralGoogle Scholar
  23. Brüssow H, Probst A, Frémont M, Sidoti J. Distinct Streptococcus thermophilus bacteriophages share an extremely conserved DNA fragment. Virology. 1994b;200(2):854–7.PubMedCrossRefGoogle Scholar
  24. Brüssow H, Canchaya C, Hardt WD. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev. 2004;68(3):560–602.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Bruttin A, Brüssow H. Site-specific spontaneous deletions in three genome regions of a temperate Streptococcus thermophilus phage. Virology. 1996;219(1):96–104.PubMedCrossRefGoogle Scholar
  26. Bruttin A, Desiere F, d’Amico N, Guérin JP, Sidoti J, Huni B, Lucchini S, Brüssow H. Molecular ecology of Streptococcus thermophilus bacteriophage infections in a cheese factory. Appl Environ Microbiol. 1997a;63(8):3144–50.PubMedPubMedCentralGoogle Scholar
  27. Bruttin A, Foley S, Brüssow H. The site-specific integration system of the temperate Streptococcus thermophilus bacteriophage phiSfi21. Virology. 1997b;237(1):148–58.PubMedCrossRefGoogle Scholar
  28. Cairns J, Stent GS, Watson JD, editors. Phage and the origins of molecular biology. New York: Cold Spring Harbor Laboratory of Quantitative Biology; 1966.Google Scholar
  29. Campbell A. General aspects of lysogeny. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 66–73.Google Scholar
  30. Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H. Prophage genomics. Microbiol Mol Biol Rev. 2003;67(2):238–76.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Casjens S, Hendrix R. Comments on the arrangement of the morphogenetic genes of bacteriophage lambda. J Mol Biol. 1974;90(1):20–5.PubMedCrossRefGoogle Scholar
  32. Castro-Nallar E, Chen H, Gladman S, Moore SC, Seemann T, Powell IB, Hillier A, Crandall KA, Chandry PS. Population genomics and phylogeography of an Australian dairy factory derived lytic bacteriophage. Genome Biol Evol. 2012;4(3):382–93.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Cavanagh D, Guinane CM, Neve H, Coffey A, Ross RP, Fitzgerald GF, McAuliffe O. Phages of non-dairy lactococci: isolation and characterization of ΦL47, a phage infecting the grass isolate Lactococcus lactis ssp. cremoris DPC6860. Front Microbiol. 2014;4:417.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cavanagh D, Fitzgerald GF, McAuliffe O. From field to fermentation: the origins of Lactococcus lactis and its domestication to the dairy environment. Food Microbiol. 2015;47:45–61.PubMedCrossRefGoogle Scholar
  35. Chandry PS, Davidson BE, Hillier AJ. Temporal transcription map of the Lactococcus lactis bacteriophage sk1. Microbiology. 1994;140(Pt 9):2251–61.PubMedCrossRefGoogle Scholar
  36. Chen JS, Dagdas YS, Kleinstiver BP, Welch MM, Sousa AA, Harrington LB, Sternberg SH, Joung JK, Yildiz A, Doudna JA. Enhanced proofreading governs CRISPR-Cas9 targeting accuracy. Nature. 2017;550(7676):407–10.ADSPubMedCrossRefGoogle Scholar
  37. Childs LM, England WE, Young MJ, Weitz JS, Whitaker RJ. CRISPR-induced distributed immunity in microbial populations. PLoS One. 2014;9(7):e101710.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  38. Chopin A, Bolotin A, Sorokin A, Ehrlich SD, Chopin M. Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. Nucleic Acids Res. 2001;29(3):644–51.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chopin A, Deveau H, Ehrlich SD, Moineau S, Chopin MC. KSY1, a lactococcal phage with a T7-like transcription. Virology. 2007;365(1):1–9.PubMedCrossRefGoogle Scholar
  40. Chou WC, Huang SC, Chiu CH, Chen YM. YMC-2011, a temperate phage of streptococcus salivarius 57.I. Appl Environ Microbiol. 2017;83(6):e03186–16.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Coles VJ, Stukel MR, Brooks MT, Burd A, Crump BC, et al. Ocean biogeochemistry modeled with emergent trait-based genomics. Science. 2017;358(6367):1149–54.ADSPubMedCrossRefGoogle Scholar
  42. Desiere F, Lucchini S, Bruttin A, Zwahlen MC, Brüssow H. A highly conserved DNA replication module from Streptococcus thermophilus phages is similar in sequence and topology to a module from Lactococcus lactis phages. Virology. 1997;234(2):372–82.PubMedCrossRefGoogle Scholar
  43. Desiere F, Lucchini S, Brüssow H. Evolution of Streptococcus thermophilus bacteriophage genomes by modular exchanges followed by point mutations and small deletions and insertions. Virology. 1998;241(2):345–56.PubMedCrossRefGoogle Scholar
  44. Desiere F, Lucchini S, Brüssow H. Comparative sequence analysis of the DNA packaging, head, and tail morphogenesis modules in the temperate cos-site Streptococcus thermophilus bacteriophage Sfi21. Virology. 1999;260(2):244–53.PubMedCrossRefGoogle Scholar
  45. Desiere F, McShan WM, van Sinderen D, Ferretti JJ, Brüssow H. Comparative genomics reveals close genetic relationships between phages from dairy bacteria and pathogenic streptococci: evolutionary implications for prophage-host interactions. Virology. 2001a;288(2):325–41.PubMedCrossRefGoogle Scholar
  46. Desiere F, Mahanivong C, Hillier AJ, Chandry PS, Davidson BE, Brüssow H. Comparative genomics of lactococcal phages: insight from the complete genome sequence of Lactococcus lactis phage BK5-T. Virology. 2001b;283(2):240–52.PubMedCrossRefGoogle Scholar
  47. Deveau H, Labrie SJ, Chopin MC, Moineau S. Biodiversity and classification of lactococcal phages. Appl Environ Microbiol. 2006;72(6):4338–46.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Doolittle WF. Phylogenetic classification and the universal tree. Science. 1999;284(5423):2124–9.PubMedCrossRefGoogle Scholar
  49. Dupuis ME, Moineau S. Genome organization and characterization of the virulent lactococcal phage 1358 and its similarities to Listeria phages. Appl Environ Microbiol. 2010;76(5):1623–32.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Dupuis MÈ, Villion M, Magadán AH, Moineau S. CRISPR-Cas and restriction-modification systems are compatible and increase phage resistance. Nat Commun. 2013;4:2087.PubMedCrossRefGoogle Scholar
  51. Eraclio G, Tremblay DM, Lacelle-Côté A, Labrie SJ, Fortina MG, Moineau S. A virulent phage infecting Lactococcus garvieae, with homology to Lactococcus lactis phages. Appl Environ Microbiol. 2015;81(24):8358–65.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Eraclio G, Fortina MG, Labrie SJ, Tremblay DM, Moineau S. Characterization of prophages of Lactococcus garvieae. Sci Rep. 2017;7(1):1856.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  53. Evershed RP, Payne S, Sherratt AG, Copley MS, Coolidge J, Urem-Kotsu D, Kotsakis K, Ozdoğan M, Ozdoğan AE, Nieuwenhuyse O, Akkermans PM, Bailey D, Andeescu RR, Campbell S, Farid S, Hodder I, Yalman N, Ozbaşaran M, Biçakci E, Garfinkel Y, Levy T, Burton MM. Earliest date for milk use in the near east and southeastern Europe linked to cattle herding. Nature. 2008;455(7212):528–31.ADSPubMedCrossRefGoogle Scholar
  54. Faber F, Tran L, Byndloss MX, Lopez CA, Velazquez EM, et al. Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion. Nature. 2016;534(7609):697–9.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  55. Filée J, Tétart F, Suttle CA, Krisch HM. Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci U S A. 2005;102(35):12471–6.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  56. Foley S, Bruttin A, Brüssow H. Widespread distribution of a group I intron and its three deletion derivatives in the lysin gene of Streptococcus thermophilus bacteriophages. J Virol. 2000;74(2):611–8.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Fortier LC, Bransi A, Moineau S. Genome sequence and global gene expression of Q54, a new phage species linking the 936 and c2 phage species of Lactococcus lactis. J Bacteriol. 2006;188(17):6101–14.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Garneau JE, Tremblay DM, Moineau S. Characterization of 1706, a virulent phage from Lactococcus lactis with similarities to prophages from other Firmicutes. Virology. 2008;373(2):298–309.PubMedCrossRefGoogle Scholar
  59. Garneau JE, Dupuis MÈ, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature. 2010;468(7320):67–71.ADSPubMedCrossRefGoogle Scholar
  60. Gasiunas G, Barrangou R, Horvath P, Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A. 2012;109(39):E2579–86.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  61. Ghasemi SM, Bouzari M, Yoon BH, Chang HI. Comparative genomic analysis of Lactococcus garvieae phage WP-2, a new member of Picovirinae subfamily of Podoviridae. Gene. 2014;551(2):222–9.PubMedCrossRefGoogle Scholar
  62. Gottesman M, Oppenheim A. Lysogeny and prophage. In: Granoff A, Webster RG, editors. Encyclopedia of virology. 2nd ed. San Diego: Academic Press; 1999. p. 925–33.CrossRefGoogle Scholar
  63. Grose JH, Casjens SR. Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology. 2014;468–470:421–43.Google Scholar
  64. Hayes S, Mahony J, Nauta A, van Sinderen D. Metagenomic approaches to assess bacteriophages in various environmental niches. Virus. 2017;9(6):E127.CrossRefGoogle Scholar
  65. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci U S A. 1999;96(5):2192–7.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  66. Hill C, Miller LA, Klaenhammer TR. In vivo genetic exchange of a functional domain from a type II A methylase between lactococcal plasmid pTR2030 and a virulent bacteriophage. J Bacteriol. 1991;173(14):4363–70.Google Scholar
  67. Hoai TD, Nishiki I, Yoshida T. Properties and genomic analysis of Lactococcus garvieae lysogenic bacteriophage PLgT-1, a new member of Siphoviridae, with homology to Lactococcus lactis phages. Virus Res. 2016;222:13–23.PubMedCrossRefGoogle Scholar
  68. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, Guédon E, Monnet V, Renault P, Kleerebezem M. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev. 2005;29(3):435–63.PubMedGoogle Scholar
  69. Horvath P, Romero DA, Coûté-Monvoisin AC, Richards M, Deveau H, Moineau S, Boyaval P, Fremaux C, Barrangou R. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol. 2008;190(4):1401–12.PubMedCrossRefGoogle Scholar
  70. Hynes AP, Villion M, Moineau S. Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages. Nat Commun. 2014;5:4399.ADSPubMedCrossRefGoogle Scholar
  71. Jarvis AW. Differentiation of lactic streptococcal phages into phage species by DNA-DNA homology. Appl Environ Microbiol. 1984;47(2):343–9.PubMedPubMedCentralGoogle Scholar
  72. Josephsen J, Andersen N, Behrndt E, Brandsborg E, Christinasen G, Hansen MB, Hansen S, Nielsen EW, Vogensen FK. An ecological study of lytic bacteriophages of Lactococcus lactis subsp. Cremoris isolated in a cheese plant over a five year period. Int Dairy J. 1994;4:123–40.CrossRefGoogle Scholar
  73. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol. 2000;299(1):27–51.PubMedCrossRefGoogle Scholar
  74. Karvelis T, Gasiunas G, Miksys A, Barrangou R, Horvath P, Siksnys V. crRNA and tracrRNA guide Cas9-mediated DNA interference in Streptococcus thermophilus. RNA Biol. 2013;10(5):841–51.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kazlauskiene M, Tamulaitis G, Kostiuk G, Venclovas Č, Siksnys V. Spatiotemporal control of type III-A CRISPR-Cas immunity: coupling DNA degradation with the target RNA recognition. Mol Cell. 2016;62(2):295–306.PubMedCrossRefGoogle Scholar
  76. Kazlauskiene M, Kostiuk G, Venclovas Č, Tamulaitis G, Siksnys V. A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems. Science. 2017;357(6351):605–9.ADSPubMedCrossRefGoogle Scholar
  77. Kelleher P, Bottacini F, Mahony J, Kilcawley KN, van Sinderen D. Comparative and functional genomics of the Lactococcus lactis taxon; insights into evolution and niche adaptation. BMC Genomics. 2017;18(1):267.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kelly WJ, Altermann E, Lambie SC, Leahy SC. Interaction between the genomes of Lactococcus lactis and phages of the P335 species. Front Microbiol. 2013;4:257.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kieser S, Sarker SA, Berger B, Sultana S, Chisti MJ, et al. Antibiotic treatment leads to fecal Escherichia coli and coliphage expansion in severely malnourished diarrhea patients. Cell Mol Gastroenterol Hepatol. 2018.  https://doi.org/10.1016/j.jcmgh.2017.11.014. (in press).
  80. Koonin EV, Wolf YI. Evolution of the CRISPR-Cas adaptive immunity systems in prokaryotes: models and observations on virus-host coevolution. Mol BioSyst. 2015;11(1):20–7.PubMedCrossRefGoogle Scholar
  81. Kot W, Neve H, Vogensen FK, Heller KJ, Sørensen SJ, Hansen LH. Complete genome sequences of four novel Lactococcus lactis phages distantly related to the rare 1706 phage species. Genome Announc. 2014;2(4):e00265–14.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kotsonis SE, Powell IB, Pillidge CJ, Limsowtin GK, Hillier AJ, Davidson BE. Characterization and genomic analysis of phage asccphi28, a phage of the family Podoviridae infecting Lactococcus lactis. Appl Environ Microbiol. 2008;74(11):3453–60.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK, Sullivan MB, Rumnieks J, Prangishvili D, Lavigne R, Kropinski AM, Klumpp J, Gillis A, Enault F, Edwards RA, Duffy S, Clokie MR, Barylski J, Ackermann HW, Kuhn JH. Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol. 2016;161(4):1095–9.PubMedCrossRefGoogle Scholar
  84. Kwan T, Liu J, DuBow M, Gros P, Pelletier J. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci U S A. 2005;102(14):5174–9.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  85. Labrie SJ, Josephsen J, Neve H, Vogensen FK, Moineau S. Morphology, genome sequence, and structural proteome of type phage P335 from Lactococcus lactis. Appl Environ Microbiol. 2008;74(15):4636–44.Google Scholar
  86. Labrie SJ, Moineau S. Abortive infection mechanisms and prophage sequences significantly influence the genetic makeup of emerging lytic lactococcal phages. J Bacteriol. 2007;189(4):1482–7.PubMedCrossRefGoogle Scholar
  87. Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol. 2010;8(5):317–27.PubMedCrossRefGoogle Scholar
  88. Labrie SJ, Tremblay DM, Moisan M, Villion M, Magadán AH, Campanacci V, Cambillau C, Moineau S. Involvement of the major capsid protein and two early-expressed phage genes in the activity of the lactococcal abortive infection mechanism AbiT. Appl Environ Microbiol. 2012;78(19):6890–9.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Le Marrec C, van Sinderen D, Walsh L, Stanley E, Vlegels E, Moineau S, Heinze P, Fitzgerald G, Fayard B. Two groups of bacteriophages infecting Streptococcus thermophilus can be distinguished on the basis of mode of packaging and genetic determinants for major structural proteins. Appl Environ Microbiol. 1997;63(8):3246–53.PubMedPubMedCentralGoogle Scholar
  90. Lenski RE. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations. ISME J. 2017;11(10):2181–94.PubMedCrossRefGoogle Scholar
  91. 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(3):e1003312.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Little JW. Gene regulatory circuitry of phage λ. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 74–82.Google Scholar
  93. Lubbers MW, Waterfield NR, Beresford TP, Le Page RW, Jarvis AW. Sequencing and analysis of the prolate-headed lactococcal bacteriophage c2 genome and identification of the structural genes. Appl Environ Microbiol. 1995;61(12):4348–56.PubMedPubMedCentralGoogle Scholar
  94. Lucchini S, Desiere F, Brüssow H. The structural gene module in Streptococcus thermophilus bacteriophage phi Sfi11 shows a hierarchy of relatedness to Siphoviridae from a wide range of bacterial hosts. Virology. 1998;246(1):63–73.PubMedCrossRefGoogle Scholar
  95. Lucchini S, Desiere F, Brüssow H. Comparative genomics of Streptococcus thermophilus phage species supports a modular evolution theory. J Virol. 1999a;73(10):8647–56.PubMedPubMedCentralGoogle Scholar
  96. Lucchini S, Desiere F, Brüssow H. Similarly organized lysogeny modules in temperate Siphoviridae from low GC content gram-positive bacteria. Virology. 1999b;263(2):427–35.PubMedCrossRefGoogle Scholar
  97. Mahony J, Martel B, Tremblay DM, Neve H, Heller KJ, Moineau S, van Sinderen D. Identification of a new P335 subgroup through molecular analysis of lactococcal phages Q33 and BM13. Appl Environ Microbiol. 2013;79(14):4401–9.Google Scholar
  98. Mahony J, van Sinderen D. Current taxonomy of phages infecting lactic acid bacteria. Front Microbiol. 2014;5:7.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Mahony J, Randazzo W, Neve H, Settanni L, van Sinderen D. Lactococcal 949 group phages recognize a carbohydrate receptor on the host cell surface. Appl Environ Microbiol. 2015;81(10):3299–305.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Mahony J, Cambillau C, van Sinderen D. Host recognition by lactic acid bacterial phages. FEMS Microbiol Rev. 2017a;41(Supp 1):S16–26.PubMedCrossRefGoogle Scholar
  101. Mahony J, Moscarelli A, Kelleher P, Lugli GA, Ventura M, Settanni L, van Sinderen D. Phage biodiversity in artisanal cheese wheys reflects the complexity of the fermentation process. Virus. 2017b;9(3):E45.CrossRefGoogle Scholar
  102. Maniloff J, Ackermann HW, Jarvis A. Phage taxonomy and classification. In: Granoff A, Webster RG, editors. Encyclopedia of virology. 2nd ed. San Diego: Academic Press; 1999. p. 1221–8.CrossRefGoogle Scholar
  103. McDonnell B, Mahony J, Neve H, Hanemaaijer L, Noben JP, Kouwen T, van Sinderen D. Identification and analysis of a novel group of bacteriophages infecting the lactic acid bacterium Streptococcus thermophilus. Appl Environ Microbiol. 2016;82(17):5153–65.PubMedPubMedCentralCrossRefGoogle Scholar
  104. McGrath S, Fitzgerald GF, van Sinderen D. Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol Microbiol. 2002;43(2):509–20.PubMedCrossRefGoogle Scholar
  105. Millen AM, Romero DA. Genetic determinants of lactococcal C2viruses for host infection and their role in phage evolution. J Gen Virol. 2016;97(8):1998–2007.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Mills S, Griffin C, Coffey A, Meijer WC, Hafkamp B, Ross RP. CRISPR analysis of bacteriophage-insensitive mutants (BIMs) of industrial Streptococcus thermophilus – implications for starter design. J Appl Microbiol. 2010;108(3):945–55.PubMedCrossRefGoogle Scholar
  107. Mills S, Griffin C, O’Sullivan O, Coffey A, McAuliffe OE, Meijer WC, Serrano LM, Ross RP. A new phage on the ‘Mozzarella’ block: bacteriophage 5093 shares a low level of homology with other Streptococcus thermophilus phages. Int Dairy J. 2011;21:963–9.CrossRefGoogle Scholar
  108. Moineau S, Fortier J, Ackermann HW, Pandian S. Characterization of lactococcal bacteriophages from Quebec cheese plants. Can J Microbiol. 1992;38:875–82.CrossRefGoogle Scholar
  109. Moineau S, Pandian S, Klaenhammer TR. Evolution of a Lytic Bacteriophage via DNA Acquisition from the Lactococcus lactis Chromosome. Appl Environ Microbiol. 1994;60(6):1832–41.Google Scholar
  110. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology. 2009;155(Pt 3):733–40.PubMedGoogle Scholar
  111. Muhammed MK, Kot W, Neve H, Mahony J, Castro-Mejía JL, Krych L, Hansen LH, Nielsen DS, Sørensen SJ, Heller KJ, van Sinderen D, Vogensen FK. Metagenomic analysis of dairy bacteriophages: extraction method and pilot study on whey samples derived from using undefined and defined mesophilic starter cultures. Appl Environ Microbiol. 2017;83(19):e00888–17.PubMedCrossRefGoogle Scholar
  112. Murphy J, Bottacini F, Mahony J, Kelleher P, Neve H, Zomer A, Nauta A, van Sinderen D. Comparative genomics and functional analysis of the 936 group of lactococcal Siphoviridae phages. Sci Rep. 2016;6:21345.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  113. Niewoehner O, Garcia-Doval C, Rostøl JT, Berk C, Schwede F, Bigler L, Hall J, Marraffini LA, Jinek M. Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers. Nature. 2017;548(7669):543–8.ADSPubMedCrossRefGoogle Scholar
  114. Oliveira J, Mahony J, Lugli GA, Hanemaaijer L, Kouwen T, Ventura M, van Sinderen D. Genome sequences of eight prophages isolated from Lactococcus lactis dairy strains. Genome Announc. 2016;4(6):e00906–16.PubMedPubMedCentralGoogle Scholar
  115. Paez-Espino D, Morovic W, Sun CL, Thomas BC, Ueda K, Stahl B, Barrangou R, Banfield JF. Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat Commun. 2013;4:1430.PubMedCrossRefGoogle Scholar
  116. Paez-Espino D, Sharon I, Morovic W, Stahl B, Thomas BC, Barrangou R, Banfield JF. CRISPR immunity drives rapid phage genome evolution in Streptococcus thermophilus. MBio. 2015;6(2):e00262–15.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, Rubin E, Ivanova NN, Kyrpides NC. Uncovering earth’s virome. Nature. 2016;536(7617):425–30.ADSPubMedCrossRefGoogle Scholar
  118. Passerini D, Beltramo C, Coddeville M, Quentin Y, Ritzenthaler P, Daveran-Mingot M-L, Le Bourgeois P. Genes but not genomes reveal bacterial domestication of Lactococcus lactis. PLoS One. 2010;5(12):e15306.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  119. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, Brucker W, Kumar V, Kandasamy J, Keenan L, Bardarov S, Kriakov J, Lawrence JG, Jacobs WR Jr, Hendrix RW, Hatfull GF. Origins of highly mosaic mycobacteriophage genomes. Cell. 2003;113(2):171–82.PubMedCrossRefGoogle Scholar
  120. Petrov VM, Ratnayaka S, Nolan JM, Miller ES, Karam JD. Genomes of the T4-related bacteriophages as windows on microbial genome evolution. Virol J. 2010;7:292.PubMedPubMedCentralCrossRefGoogle Scholar
  121. Pietilä MK, Laurinmäki P, Russell DA, Ko CC, Jacobs-Sera D, Hendrix RW, Bamford DH, Butcher SJ. Structure of the archaeal head-tailed virus HSTV-1 completes the HK97 fold story. Proc Natl Acad Sci U S A. 2013;110(26):10604–9.ADSPubMedPubMedCentralCrossRefGoogle Scholar
  122. Pope WH, Bowman CA, Russell DA, Jacobs-Sera D, Asai DJ, Cresawn SG, Jacobs WR, Hendrix RW, Lawrence JG, Hatfull GF, Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science, Phage Hunters Integrating Research and Education, Mycobacterial Genetics Course. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. elife. 2015;4:e06416.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Prevots F, Mata M, Ritzenthaler P. Taxonomic differentiation of 101 lactococcal bacteriophages and characterization of bacteriophages with unusually large genomes. Appl Environ Microbiol. 1990;56(7):2180–5.PubMedPubMedCentralGoogle Scholar
  124. Proux C, van Sinderen D, Suarez J, Garcia P, Ladero V, Fitzgerald GF, Desiere F, Brüssow H. The dilemma of phage taxonomy illustrated by comparative genomics of Sfi21-like Siphoviridae in lactic acid bacteria. J Bacteriol. 2002;184(21):6026–36.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Quiberoni A, Tremblay D, Ackermann HW, Moineau S, Reinheimer JA. Diversity of Streptococcus thermophilus phages in a large-production cheese factory in Argentina. J Dairy Sci. 2006;89(10):3791–9.PubMedCrossRefGoogle Scholar
  126. Rakonjac J, O’Toole PW, Lubbers M. Isolation of lactococcal prolate phage-phage recombinants by an enrichment strategy reveals two novel host range determinants. J Bacteriol. 2005;187(9):3110–21.PubMedPubMedCentralCrossRefGoogle Scholar
  127. Rohwer F. Global phage diversity. Cell. 2003;113(2):141.PubMedCrossRefGoogle Scholar
  128. Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, Poulos BT, Solonenko N, Lara E, Poulain J, Pesant S, Kandels-Lewis S, Dimier C, Picheral M, Searson S, Cruaud C, Alberti A, Duarte CM, Gasol JM, Vaqué D, Tara Oceans Coordinators, Bork P, Acinas SG, Wincker P, Sullivan MB. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature. 2016;537(7622):689–93.PubMedCrossRefGoogle Scholar
  129. Samson JE, Moineau S. Characterization of Lactococcus lactis phage 949 and comparison with other lactococcal phages. Appl Environ Microbiol. 2010;76(20):6843–52.Google Scholar
  130. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 2011;39(21):9275–82.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Sarker SA, McCallin S, Barretto C, Berger B, Pittet AC, Sultana S, Krause L, Huq S, Bibiloni R, Bruttin A, Reuteler G, Brüssow H. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology. 2012;434(2):222–32.PubMedCrossRefGoogle Scholar
  132. Sarker SA, Berger B, Deng Y, Kieser S, Foata F, et al. Oral application of Escherichia coli bacteriophage: safety tests in healthy and diarrheal children from Bangladesh. Environ Microbiol. 2017;19(1):237–50.PubMedCrossRefGoogle Scholar
  133. Siezen RJ, Starrenburg MJC, Boekhorst J, Renckens B, Molenaar D, van Hylckama Vlieg JET. Genome-scale genotype-phenotype matching of two Lactococcus lactis isolates from plants identifies mechanisms of adaptation to the plant niche. Appl Environ Microbiol. 2008;74(2):424–36.PubMedCrossRefGoogle Scholar
  134. Stahl FW, Murray NE. The evolution of gene clusters and genetic circularity in microorganisms. Genetics. 1966;53(3):569–76.PubMedPubMedCentralGoogle Scholar
  135. Stanley E, Walsh L, van der Zwet A, Fitzgerald GF, van Sinderen D. Identification of four loci isolated from two Streptococcus thermophilus phage genomes responsible for mediating bacteriophage resistance. FEMS Microbiol Lett. 2000;182(2):271–7.PubMedCrossRefGoogle Scholar
  136. Sun CL, Barrangou R, Thomas BC, Horvath P, Fremaux C, Banfield JF. Phage mutations in response to CRISPR diversification in a bacterial population. Environ Microbiol. 2013;15(2):463–70.PubMedCrossRefGoogle Scholar
  137. Szymczak P, Janzen T, Neves AR, Kot W, Hansen LH, Lametsch R, Neve H, Franz CM, Vogensen FK. Novel variants of Streptococcus thermophilus bacteriophages are indicative of genetic recombination among phages from different bacterial species. Appl Environ Microbiol. 2017;83(5):e02748–16.PubMedPubMedCentralCrossRefGoogle Scholar
  138. Vale PF, Lafforgue G, Gatchitch F, Gardan R, Moineau S, Gandon S. Costs of CRISPR-Cas-mediated resistance in Streptococcus thermophilus. Proc Biol Sci. 2015;282(1812):20151270.PubMedPubMedCentralCrossRefGoogle Scholar
  139. van Sinderen D, Karsens H, Kok J, Terpstra P, Ruiters MH, Venema G, Nauta A. Sequence analysis and molecular characterization of the temperate lactococcal bacteriophage r1t. Mol Microbiol. 1996;19(6):1343–55.PubMedCrossRefGoogle Scholar
  140. Villarreal LP. Are viruses alive? Sci Am. 2004;291(6):100–5.PubMedCrossRefGoogle Scholar
  141. Villion M, Chopin MC, Deveau H, Ehrlich SD, Moineau S, Chopin A. P087, a lactococcal phage with a morphogenesis module similar to an enterococcus faecalis prophage. Virology. 2009;388(1):49–56.PubMedCrossRefGoogle Scholar
  142. Wommack KE, Colwell RR. Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev. 2000;64(1):69–114.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Division of Animal and Human Health Engineering, Laboratory of Gene TechnologyUniversity of LeuvenLeuvenBelgium

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