1887

Abstract

SAR11 bacteria dominate ocean surface bacterioplankton communities, and play an important role in marine carbon and nutrient cycling. The biology and ecology of SAR11 are impacted by SAR11 phages (pelagiphages) that are highly diverse and abundant in the ocean. Among the currently known pelagiphages, HTVC010P represents an extremely abundant but under-studied phage group in the ocean. In this study, we have isolated seven new HTVC010P-type pelagiphages, and recovered 77 nearly full-length HTVC010P-type metagenomic viral genomes from marine metagenomes. Comparative genomic and phylogenomic analyses showed that HTVC010P-type pelagiphages display genome synteny and can be clustered into two major subgroups, with subgroup I consisting of strictly lytic phages and subgroup II mostly consisting of phages with potential lysogenic life cycles. All but one member of the subgroup II contain an integrase gene. Site-specific integration of subgroup II HTVC010P-type pelagiphage was either verified experimentally or identified by genomic sequence analyses, which revealed that various SAR11 tRNA genes can serve as the integration sites of HTVC010P-type pelagiphages. Moreover, HTVC010P-type pelagiphage integration was confirmed by the detection of several Global Ocean Survey (GOS) fragments that contain hybrid phage–host integration sites. Metagenomic recruitment analysis revealed that these HTVC010P-type phages were globally distributed and most lytic subgroup I members exhibited higher relative abundance. Altogether, this study significantly expands our knowledge about the genetic diversity, life strategies and ecology of HTVC010P-type pelagiphages.

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2021-07-06
2021-07-29
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References

  1. Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature 1999; 399:541–548 [View Article] [PubMed]
    [Google Scholar]
  2. Wommack KE, Colwell RR. Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 2000; 64:69–114 [View Article] [PubMed]
    [Google Scholar]
  3. Suttle CA. Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 2007; 5:801–812 [View Article] [PubMed]
    [Google Scholar]
  4. Suttle CA. Viruses in the sea. Nature 2005; 437:356–361 [View Article] [PubMed]
    [Google Scholar]
  5. Wilhelm SW, Suttle CA. Viruses and nutrient cycles in the Sea. Bioscience 1999; 49:781–788
    [Google Scholar]
  6. Feiner R, Argov T, Rabinovich L, Sigal N, Borovok I et al. A new perspective on lysogeny: Prophages as active regulatory switches of bacteria. Nat Rev Microbiol 2015; 13:641–650 [View Article] [PubMed]
    [Google Scholar]
  7. Correa AMS, Howard-Varona C, Coy SR, Buchan A, Sullivan MB et al. Revisiting the rules of life for viruses of microorganisms. Nat Rev Microbiol 2021 [View Article] [PubMed]
    [Google Scholar]
  8. Weinbauer MG. Ecology of prokaryotic viruses. FEMS Microbiol Rev 2004; 28:127–181 [View Article] [PubMed]
    [Google Scholar]
  9. Sime-Ngando T. Environmental bacteriophages: viruses of microbes in aquatic ecosystems. Front Microbiol 2014; 5:355 [View Article] [PubMed]
    [Google Scholar]
  10. Howard-Varona C, Hargreaves KR, Abedon ST, Sullivan MB. Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J 2017; 11:1511–1520 [View Article] [PubMed]
    [Google Scholar]
  11. Paul JH. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas. ISME J 2008; 2:579–589 [View Article] [PubMed]
    [Google Scholar]
  12. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL et al. Abundant SAR11 viruses in the ocean. Nature 2013; 494:357–360 [View Article] [PubMed]
    [Google Scholar]
  13. Kang I, Oh HM, Kang D, Cho JC. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc Natl Acad Sci U S A 2013; 110:12343–12348 [View Article]
    [Google Scholar]
  14. Zhang Z, Chen F, Chu X, Zhang H, Luo H et al. Diverse, abundant, and novel viruses infecting the marine roseobacter RCA lineage. mSystems 2019; 4:e00494–19 [View Article]
    [Google Scholar]
  15. Zhang Z, Qin F, Chen F, Chu X, Luo H et al. Culturing novel and abundant pelagiphages in the ocean. Environ Microbiol 2021; 23:1145–1161 [View Article]
    [Google Scholar]
  16. Buchholz HH, Michelsen ML, Bolaños LM, Browne E, Allen MJ et al. Efficient dilution-to-extinction isolation of novel virus-host model systems for fastidious heterotrophic bacteria. ISME J 2021 [View Article] [PubMed]
    [Google Scholar]
  17. Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 2002; 420:806–810 [View Article] [PubMed]
    [Google Scholar]
  18. Giovannoni SJ. SAR11 bacteria: the most abundant plankton in the oceans. Ann Rev Mar Sci 2017; 9:231–255 [View Article] [PubMed]
    [Google Scholar]
  19. Zhao Y, Qin F, Zhang R, Giovannoni SJ, Zhang Z et al. Pelagiphages in the Podoviridae family integrate into host genomes. Environ Microbiol 2019; 21:1989–2001 [View Article] [PubMed]
    [Google Scholar]
  20. Morris RM, Cain KR, Hvorecny KL, Kollman JM. Lysogenic host-virus interactions in SAR11 marine bacteria. Nat Microbiol 2020; 5:1011–1015 [View Article] [PubMed]
    [Google Scholar]
  21. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. Expanding the marine virosphere using metagenomics. PLoS Genet 2013; 9:e1003987 [View Article]
    [Google Scholar]
  22. Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 2016; 537:689–693 [View Article] [PubMed]
    [Google Scholar]
  23. Gregory AC, Zayed AA, Conceição-Neto N, Temperton B, Bolduc B et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell 2019; 177:1109–1123 [View Article] [PubMed]
    [Google Scholar]
  24. Beaulaurier J, Luo E, Eppley JM, Uyl PD, Dai X et al. Assembly-free single-molecule sequencing recovers complete virus genomes from natural microbial communities. Genome Res 2020; 30:437–446 [View Article] [PubMed]
    [Google Scholar]
  25. Zaragoza-Solas A, Rodriguez-Valera F, López-Pérez M. Metagenome mining reveals hidden genomic diversity of pelagimyophages in aquatic environments. mSystems 2020; 5:00919–e00905 [View Article]
    [Google Scholar]
  26. Martinez-Hernandez F, Fornas O, Lluesma Gomez M, Bolduc B, de la Cruz Peña MJ et al. Single-virus genomics reveals hidden cosmopolitan and abundant viruses. Nat Commun 2017; 8:15892 [View Article] [PubMed]
    [Google Scholar]
  27. Martinez-Hernandez F, Garcia-Heredia I, Lluesma Gomez M, Maestre-Carballa L, Martínez Martínez J et al. Droplet digital PCR for estimating absolute abundances of widespread pelagibacter viruses. Front Microbiol 2019; 10:1226 [View Article] [PubMed]
    [Google Scholar]
  28. Eggleston EM, Hewson I. Abundance of two pelagibacter ubique bacteriophage genotypes along a latitudinal transect in the North and South Atlantic oceans. Front Microbiol 2016; 7:1534 [View Article] [PubMed]
    [Google Scholar]
  29. Warwick-Dugdale J, Solonenko N, Moore K, Chittick L, Gregory AC et al. Long-read viral metagenomics captures abundant and microdiverse viral populations and their niche-defining genomic islands. PeerJ 2019; 7:e6800 [View Article] [PubMed]
    [Google Scholar]
  30. Chen L-X, Zhao Y, McMahon KD, Mori JF, Jessen GL et al. Wide distribution of phage that infect freshwater SAR11 bacteria. mSystems 2019; 4:e00410–19 [View Article]
    [Google Scholar]
  31. Carini P, Steindler L, Beszteri S, Giovannoni SJ. Nutrient requirements for growth of the extreme oligotroph “Candidatus Pelagibacter ubique” HTCC1062 on a defined medium. ISME J 2013; 7:592–602 [View Article] [PubMed]
    [Google Scholar]
  32. Connon SA, Giovannoni SJ. High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 2002; 68:3878–3885 [View Article] [PubMed]
    [Google Scholar]
  33. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1989
    [Google Scholar]
  34. Lukashin AV, Borodovsky M. Genemark.Hmm: New solutions for gene finding. Nucleic Acids Res 1998; 26:1107–1115 [View Article]
    [Google Scholar]
  35. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  36. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY et al. Pfam: The protein families database. Nucleic Acids Res 2014; 42:D222–D230 [View Article] [PubMed]
    [Google Scholar]
  37. Zdobnov EM, Apweiler R. InterProScan – an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001; 17:847–848 [View Article] [PubMed]
    [Google Scholar]
  38. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK et al. CDD: A conserved domain database for the functional annotation of proteins. Nucleic Acids Res 2011; 39:D225–D229 [View Article] [PubMed]
    [Google Scholar]
  39. Söding J, Biegert A, Lupas AN. The Hhpred Interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005; 33:W244–W248 [View Article] [PubMed]
    [Google Scholar]
  40. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article] [PubMed]
    [Google Scholar]
  41. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article] [PubMed]
    [Google Scholar]
  42. Fischer S, Brunk BP, Chen F, Gao X, Harb OS et al. Using Orthomcl to assign proteins to orthomcl-db groups or to cluster proteomes into new ortholog groups. Curr Protoc Bioinformatics 2011; 35:6–12
    [Google Scholar]
  43. Lavigne R, Seto D, Mahadevan P, Ackermann HW, Kropinski AM. Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 2008; 159:406–414 [View Article] [PubMed]
    [Google Scholar]
  44. Katoh K, Asimenos G, Toh H. Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 2009; 537:39–64 [View Article] [PubMed]
    [Google Scholar]
  45. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  46. Meier-Kolthoff JP, Goker M. VICTOR: genome-based phylogeny and classification of prokaryotic viruses. Bioinformatics 2017; 33:3396–3404 [View Article] [PubMed]
    [Google Scholar]
  47. Eddy SR. Profile hidden Markov models. Bioinformatics 1998; 14:755–763 [View Article] [PubMed]
    [Google Scholar]
  48. Fuller RS, Funnell BE, Kornberg A. The dnAA protein complex with the E. Coli chromosomal replication origin (ORIC) and other DNA sites. Cell 1984; 3:889–990
    [Google Scholar]
  49. Wegrzyn G, Szalewska-Pałasz A, Wegrzyn A, Obuchowski M, Taylor KJG. Transcriptional activation of the origin of coliphage λ DNA replication is regulated by the host DnaA initiator function. Gene 1995; 154:47–50 [View Article]
    [Google Scholar]
  50. Fogg PC, Colloms S, Rosser S, Stark M, Smith MC. New applications for phage integrases. J Mol Biol 2014; 426:2703–2716 [View Article] [PubMed]
    [Google Scholar]
  51. McDonnell GE, McConnell DJ. Overproduction, isolation, and DNA-binding characteristics of Xre, the repressor protein from the Bacillus subtilis defective prophage PBSX. J Bacteriol 1994; 176:5831–5834 [View Article] [PubMed]
    [Google Scholar]
  52. Salah Ud-Din AI, Tikhomirova A, Roujeinikova A. Structure and functional diversity of GCN5-related N-acetyltransferases (GNAT. Int J Mol Sci 2016; 17:1018 [View Article] [PubMed]
    [Google Scholar]
  53. Sabehi G, Shaulov L, Silver DH, Yanai I, Harel A et al. A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc Natl Acad Sci USA 2012; 109:2037–2042 [View Article] [PubMed]
    [Google Scholar]
  54. Murphy J, Mahony J, Ainsworth S, Nauta A, Van Sinderen D. Bacteriophage orphan DNA methyltransferases: insights from their bacterial origin, function, and occurrence. Appl Environ Microbiol 2013; 79:7547–7555 [View Article] [PubMed]
    [Google Scholar]
  55. Krone FA, Westphal G, Schwenn JD. Characterisation of the gene cysH and of its product phospho-adenylylsulphate reductase from Escherichia coli. Mol Gen Genet 1991; 225:314–319 [View Article]
    [Google Scholar]
  56. Tripp HJ, Kitner JB, Schwalbach MS, Dacey JWH, Wilhelm LJ et al. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 2008; 452:741–744 [View Article] [PubMed]
    [Google Scholar]
  57. Williams KP. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 2002; 30:866–875 [View Article]
    [Google Scholar]
  58. Knowles B, Silveira CB, Bailey BA, Barott K, Cantu VA et al. Lytic to temperate switching of viral communities. Nature 2016; 531:466–470 [View Article] [PubMed]
    [Google Scholar]
  59. Touchon M, Bernheim A, Rocha EP. Genetic and life-history traits associated with the distribution of prophages in bacteria. ISME J 2016; 10:2744–2754 [View Article] [PubMed]
    [Google Scholar]
  60. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. Three prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 2005; 3:e144 [View Article] [PubMed]
    [Google Scholar]
  61. Pope WH, Weigele PR, Chang J, Pedulla ML, Ford ME et al. Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: a “horned” bacteriophage of marine synechococcus. J Mol Biol 2007; 368:966–981 [View Article] [PubMed]
    [Google Scholar]
  62. Labrie SJ, Frois-Moniz K, Osburne MS, Kelly L, Roggensack SE et al. Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol 2013; 15:1356–1376 [View Article] [PubMed]
    [Google Scholar]
  63. Huang S, Zhang S, Jiao N, Chen F. Comparative genomic and phylogenomic analyses reveal a conserved core genome shared by estuarine and oceanic cyanopodoviruses. PLoS One 2015; 10:11
    [Google Scholar]
  64. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M et al. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial “mobilome”. Environ Microbiol 2009; 11:2935–2951 [View Article] [PubMed]
    [Google Scholar]
  65. Malmstrom RR, Rodrigue S, Huang KH, Kelly L, Kern SE et al. Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis. ISME J 2013; 7:184–198 [View Article] [PubMed]
    [Google Scholar]
  66. Flores‐Uribe J, Philosof A, Sharon I, Fridman S, Larom S et al. A novel uncultured marine cyanophage lineage with lysogenic potential linked to a putative marine Synechococcus ‘relic’ prophage. Environ Microbiol Rep 2019; 11:598–604 [View Article]
    [Google Scholar]
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