Skip to main content

Population Genomics of Bacteriophages

  • Chapter
  • First Online:

Part of the book series: Population Genomics ((POGE))

Abstract

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.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Ackermann HW. Bacteriophage observations and evolution. Res Microbiol. 2003;154(4):245–51.

    CAS  PubMed  Google Scholar 

  • Ackermann HW. Classification of bacteriophages. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 8–16.

    Google Scholar 

  • Ackermann HW, Kropinski AM. Curated list of prokaryote viruses with fully sequenced genomes. Res Microbiol. 2007;158(7):555–66.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Botstein D. A theory of modular evolution for bacteriophages. Ann N Y Acad Sci. 1980;354:484–90.

    CAS  PubMed  Google Scholar 

  • Bouchard JD, Moineau S. Homologous recombination between a lactococcal bacteriophage and the chromosome of its host strain. Virology. 2000;270(1):65–75.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Brüssow H. Phages of dairy bacteria. Annu Rev Microbiol. 2001;55:283–303.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Brüssow H, Bruttin A. Characterization of a temperate Streptococcus thermophilus bacteriophage and its genetic relationship with lytic phages. Virology. 1995;212(2):632–40.

    PubMed  Google Scholar 

  • Brüssow H, Desiere F. Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol Microbiol. 2001;39(2):213–22.

    PubMed  Google Scholar 

  • 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 

  • Brüssow H, Hendrix RW. Phage genomics: small is beautiful. Cell. 2002;108(1):13–6.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Brüssow H, Probst A, Frémont M, Sidoti J. Distinct Streptococcus thermophilus bacteriophages share an extremely conserved DNA fragment. Virology. 1994b;200(2):854–7.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Bruttin A, Brüssow H. Site-specific spontaneous deletions in three genome regions of a temperate Streptococcus thermophilus phage. Virology. 1996;219(1):96–104.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bruttin A, Foley S, Brüssow H. The site-specific integration system of the temperate Streptococcus thermophilus bacteriophage phiSfi21. Virology. 1997b;237(1):148–58.

    CAS  PubMed  Google Scholar 

  • 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 

  • Campbell A. General aspects of lysogeny. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 66–73.

    Google Scholar 

  • Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H. Prophage genomics. Microbiol Mol Biol Rev. 2003;67(2):238–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Casjens S, Hendrix R. Comments on the arrangement of the morphogenetic genes of bacteriophage lambda. J Mol Biol. 1974;90(1):20–5.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Chandry PS, Davidson BE, Hillier AJ. Temporal transcription map of the Lactococcus lactis bacteriophage sk1. Microbiology. 1994;140(Pt 9):2251–61.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Childs LM, England WE, Young MJ, Weitz JS, Whitaker RJ. CRISPR-induced distributed immunity in microbial populations. PLoS One. 2014;9(7):e101710.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Deveau H, Labrie SJ, Chopin MC, Moineau S. Biodiversity and classification of lactococcal phages. Appl Environ Microbiol. 2006;72(6):4338–46.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doolittle WF. Phylogenetic classification and the universal tree. Science. 1999;284(5423):2124–9.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eraclio G, Fortina MG, Labrie SJ, Tremblay DM, Moineau S. Characterization of prophages of Lactococcus garvieae. Sci Rep. 2017;7(1):1856.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Hayes S, Mahony J, Nauta A, van Sinderen D. Metagenomic approaches to assess bacteriophages in various environmental niches. Virus. 2017;9(6):E127.

    Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Hynes AP, Villion M, Moineau S. Adaptation in bacterial CRISPR-Cas immunity can be driven by defective phages. Nat Commun. 2014;5:4399.

    CAS  PubMed  Google Scholar 

  • Jarvis AW. Differentiation of lactic streptococcal phages into phage species by DNA-DNA homology. Appl Environ Microbiol. 1984;47(2):343–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol. 2010;8(5):317–27.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Lenski RE. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations. ISME J. 2017;11(10):2181–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Little JW. Gene regulatory circuitry of phage λ. In: Calendar R, editor. The bacteriophages. Oxford: Oxford University Press; 2006. p. 74–82.

    Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahony J, van Sinderen D. Current taxonomy of phages infecting lactic acid bacteria. Front Microbiol. 2014;5:7.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahony J, Cambillau C, van Sinderen D. Host recognition by lactic acid bacterial phages. FEMS Microbiol Rev. 2017a;41(Supp 1):S16–26.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Moineau S, Fortier J, Ackermann HW, Pandian S. Characterization of lactococcal bacteriophages from Quebec cheese plants. Can J Microbiol. 1992;38:875–82.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rohwer F. Global phage diversity. Cell. 2003;113(2):141.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Samson JE, Moineau S. Characterization of Lactococcus lactis phage 949 and comparison with other lactococcal phages. Appl Environ Microbiol. 2010;76(20):6843–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Stahl FW, Murray NE. The evolution of gene clusters and genetic circularity in microorganisms. Genetics. 1966;53(3):569–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Villarreal LP. Are viruses alive? Sci Am. 2004;291(6):100–5.

    PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Wommack KE, Colwell RR. Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev. 2000;64(1):69–114.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgment

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Harald Brüssow .

Editor information

Editors and Affiliations

Additional information

To the memory of the late Roger Hendrix and Hans Ackermann, who dedicated their scientific life to bacteriophage research.

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Brüssow, H. (2018). Population Genomics of Bacteriophages. In: Polz, M., Rajora, O. (eds) Population Genomics: Microorganisms. Population Genomics. Springer, Cham. https://doi.org/10.1007/13836_2018_16

Download citation

Publish with us

Policies and ethics