1887

Microbial Genomics logo

Volume 10, Issue 4

Genome sequences of the first phages infecting marine Open Access

Abstract

The ubiquitous and abundant marine phages play critical roles in shaping the composition and function of bacterial communities, impacting biogeochemical cycling in marine ecosystems. is among the most abundant and ubiquitous phage families in the ocean. However, studies on the diversity and ecology of phages in marine environments are restricted to isolates that infect SAR11 bacteria and cyanobacteria. In this study, ten new roseophages that infect marine strains were isolated from coastal waters. These new roseophages have a genome size ranging from 38 917 to 42 634 bp and G+C content of 44.6–50 %. Comparative genomics showed that they are similar to known phages regarding gene content and architecture, thus representing the first roseophages. Phylogenomic analysis based on concatenated conserved genes showed that the ten roseophages form three distinct subgroups within the , and sequence analysis revealed that they belong to eight new genera. Finally, viromic read-mapping showed that these new phages are widely distributed in global oceans, mostly inhabiting polar and estuarine locations. This study has expanded the current understanding of the genomic diversity, evolution and ecology of phages and roseophages. We suggest that phages play important roles in the mortality and community structure of roseobacters, and have broad ecological applications.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Autographiviridae phages , comparative genomics , distribution patterns , phylogenomic analysis and Roseobacter
Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 42206096)
    • Principle Award Recipient: ZefengZhang
  • National Natural Science Foundation of China (Award 42076105)
    • Principle Award Recipient: YanlinZhao
  • National Natural Science Foundation of China (Award 42276144)
    • Principle Award Recipient: YanlinZhao
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001240
2024-04-17
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10/4/mgen001240.html?itemId=/content/journal/mgen/10.1099/mgen.0.001240&mimeType=html&fmt=ahah

References

  1. Dion MB, Oechslin F, Moineau S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol 2020; 18:125–138 [View Article] [PubMed]
     [Google Scholar]
  2. Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat Microbiol 2018; 3:754–766 [View Article] [PubMed]
     [Google Scholar]
  3. Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature 1999; 399:541–548 [View Article] [PubMed]
     [Google Scholar]
  4. Suttle CA. Viruses in the sea. Nature 2005; 437:356–361 [View Article] [PubMed]
     [Google Scholar]
  5. Suttle CA. Marine viruses--major players in the global ecosystem. Nat Rev Microbiol 2007; 5:801–812 [View Article] [PubMed]
     [Google Scholar]
  6. Breitbart M. Marine viruses: truth or dare. Ann Rev Mar Sci 2012; 4:425–448 [View Article] [PubMed]
     [Google Scholar]
  7. Wang S, Yang Y, Jing J. A synthesis of viral contribution to marine nitrogen cycling. Front Microbiol 2022; 13:834581 [View Article] [PubMed]
     [Google Scholar]
  8. Pourtois J, Tarnita CE, Bonachela JA. Impact of lytic phages on phosphorus- vs. nitrogen-limited marine microbes. Front Microbiol 2020; 11:221 [View Article] [PubMed]
     [Google Scholar]
  9. Warwick-Dugdale J, Buchholz HH, Allen MJ, Temperton B. Host-hijacking and planktonic piracy: how phages command the microbial high seas. Virol J 2019; 16:15 [View Article] [PubMed]
     [Google Scholar]
  10. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. Expanding the marine virosphere using metagenomics. PLoS Genet 2013; 9:e1003987 [View Article] [PubMed]
     [Google Scholar]
  11. 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]
  12. Klemetsen T, Raknes IA, Fu J, Agafonov A, Balasundaram SV et al. The MAR databases: development and implementation of databases specific for marine metagenomics. Nucleic Acids Res 2018; 46:D692–D699 [View Article] [PubMed]
     [Google Scholar]
  13. 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]
  14. Pachiadaki MG, Brown JM, Brown J, Bezuidt O, Berube PM et al. Charting the complexity of the marine microbiome through single-cell genomics. Cell 2019; 179:1623–1635 [View Article] [PubMed]
     [Google Scholar]
  15. 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]
  16. 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] [PubMed]
     [Google Scholar]
  17. 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] [PubMed]
     [Google Scholar]
  18. Cai L, Chen Y, Xiao S, Liu R, He M et al. Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene. ISME J 2023; 17:252–262 [View Article] [PubMed]
     [Google Scholar]
  19. Adriaenssens EM, Sullivan MB, Knezevic P, van Zyl LJ, Sarkar BL et al. Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol 2020; 165:1253–1260 [View Article] [PubMed]
     [Google Scholar]
  20. Molineux IJ. The T7 group. In Calendar R. ed The Bacteriophages New York, USA; Oxford, UK: Oxford University Press; 2006 pp 277–301 [View Article]
     [Google Scholar]
  21. Turner D, Kropinski A, Alfernas-Zerbini P, Buttimer C, Lavigne R et al. Create one new family (Autographiviridae) including nine subfamilies and one hundred and thirty-wwo genera in the order Caudovirales Washington, DC, USA: International Committee on Taxonomy of Viruses; 2019
     [Google Scholar]
  22. Chen F, Lu J. Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. Appl Environ Microbiol 2002; 68:2589–2594 [View Article] [PubMed]
     [Google Scholar]
  23. 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]
  24. 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]
  25. 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]
  26. 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]
  27. 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:e0142962 [View Article] [PubMed]
     [Google Scholar]
  28. 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]
  29. 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; 15:1585–1598 [View Article] [PubMed]
     [Google Scholar]
  30. Moran MA, Belas R, Schell MA, González JM, Sun F et al. Ecological genomics of marine Roseobacters. Appl Environ Microbiol 2007; 73:4559–4569 [View Article] [PubMed]
     [Google Scholar]
  31. Brinkhoff T, Giebel HA, Simon M. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 2008; 189:531–539 [View Article] [PubMed]
     [Google Scholar]
  32. González JM, Kiene RP, Moran MA. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria. Appl Environ Microbiol 1999; 65:3810–3819 [View Article] [PubMed]
     [Google Scholar]
  33. Moran MA, González JM, Kiene RP. Linking a bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group. Geomicrobiol J 2003; 20:375–388 [View Article]
     [Google Scholar]
  34. Christie-Oleza JA, Armengaud J. Proteomics of the Roseobacter clade, a window to the marine microbiology landscape. Proteomics 2015; 15:3928–3942 [View Article] [PubMed]
     [Google Scholar]
  35. Zhan Y, Chen F. Bacteriophages that infect marine roseobacters: genomics and ecology. Environ Microbiol 2019; 21:1885–1895 [View Article] [PubMed]
     [Google Scholar]
  36. Bischoff V, Bunk B, Meier-Kolthoff JP, Spröer C, Poehlein A et al. Cobaviruses - a new globally distributed phage group infecting Rhodobacteraceae in marine ecosystems. ISME J 2019; 13:1404–1421 [View Article] [PubMed]
     [Google Scholar]
  37. Cai L, Ma R, Chen H, Yang Y, Jiao N et al. A newly isolated roseophage represents a distinct member of Siphoviridae family. Virol J 2019; 16:128 [View Article] [PubMed]
     [Google Scholar]
  38. 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:e00494–00419 [View Article] [PubMed]
     [Google Scholar]
  39. Zhai Z, Zhang Z, Zhao G, Liu X, Qin F et al. Genomic characterization of two novel RCA phages reveals new insights into the diversity and evolution of marine viruses. Microbiol Spectr 2021; 9:e0123921 [View Article] [PubMed]
     [Google Scholar]
  40. Qin F, Du S, Zhang Z, Ying H, Wu Y et al. Newly identified HMO-2011-type phages reveal genomic diversity and biogeographic distributions of this marine viral group. ISME J 2022; 16:1363–1375 [View Article] [PubMed]
     [Google Scholar]
  41. Stingl U, Tripp HJ, Giovannoni SJ. Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time Series study site. ISME J 2007; 1:361–371 [View Article] [PubMed]
     [Google Scholar]
  42. Cho JC, Giovannoni SJ. Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 2004; 70:432–440 [View Article] [PubMed]
     [Google Scholar]
  43. Nagasaki K, Bratbak G. Isolation of viruses infecting photosynthetic and nonphotosynthetic protists. Manual Aquat Viral Ecol 201092–101 [View Article]
     [Google Scholar]
  44. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
     [Google Scholar]
  45. Li D, Luo R, Liu C-M, Leung C-M, Ting H-F et al. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 2016; 102:3–11 [View Article] [PubMed]
     [Google Scholar]
  46. 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; 11:119–129 [View Article] [PubMed]
     [Google Scholar]
  47. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29–37 [View Article] [PubMed]
     [Google Scholar]
  48. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY et al. Pfam: the protein families database. Nucleic Acids Res 2014; 42:D222–30 [View Article] [PubMed]
     [Google Scholar]
  49. 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]
  50. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinform 2011; 27:1009–1010 [View Article] [PubMed]
     [Google Scholar]
  51. 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]
  52. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinform 2009; 25:1972–1973 [View Article] [PubMed]
     [Google Scholar]
  53. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Methods Mol Biol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  54. Nishimura Y, Yoshida T, Kuronishi M, Uehara H, Ogata H et al. ViPTree: the viral proteomic tree server. Bioinformatics 2017; 33:2379–2380 [View Article]
     [Google Scholar]
  55. Moraru C, Varsani A, Kropinski A. VIRIDIC-A novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses. Viruses 2020; 12:1268 [View Article] [PubMed]
     [Google Scholar]
  56. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
     [Google Scholar]
  57. Xu B, Li F, Cai L, Zhang R, Fan L et al. A holistic genome dataset of bacteria, archaea and viruses of the Pearl River estuary. Sci Data 2022; 9:49 [View Article] [PubMed]
     [Google Scholar]
  58. Gao C, Liang Y, Jiang Y, Paez-Espino D, Han M et al. Virioplankton assemblages from challenger deep, the deepest place in the oceans. iScience 2022; 25:104680 [View Article] [PubMed]
     [Google Scholar]
  59. Jurgensen SK, Roux S, Schwenck SM, Stewart FJ, Sullivan MB et al. Viral community analysis in a marine oxygen minimum zone indicates increased potential for viral manipulation of microbial physiological state. ISME J 2022; 16:972–982 [View Article] [PubMed]
     [Google Scholar]
  60. Sun M, Zhan Y, Marsan D, Páez-Espino D, Cai L et al. Uncultivated viral populations dominate estuarine viromes on the spatiotemporal scale. mSystems 2021; 6:e01020–01020 [View Article] [PubMed]
     [Google Scholar]
  61. Jaiani E, Kusradze I, Kokashvili T, Geliashvili N, Janelidze N et al. Microbial diversity and phage-host interactions in the Georgian Coastal Area of the Black Sea revealed by whole genome metagenomic sequencing. Mar Drugs 2020; 18:558 [View Article] [PubMed]
     [Google Scholar]
  62. Hevroni G, Flores-Uribe J, Béjà O, Philosof A. Seasonal and diel patterns of abundance and activity of viruses in the Red Sea. Proc Natl Acad Sci U S A 2020; 117:29738–29747 [View Article] [PubMed]
     [Google Scholar]
  63. Liang Y, Wang L, Wang Z, Zhao J, Yang Q et al. Metagenomic analysis of the diversity of DNA viruses in the surface and deep sea of the South China Sea. Front Microbiol 2019; 10:1951 [View Article] [PubMed]
     [Google Scholar]
  64. R K Pheatmap: pretty Heatmaps. R package version 2012
     [Google Scholar]
  65. Feng X, Chu X, Qian Y, Henson MW, Lanclos VC et al. Mechanisms driving genome reduction of a novel Roseobacter lineage. ISME J 2021; 15:3576–3586 [View Article] [PubMed]
     [Google Scholar]
  66. Myllykallio H, Lipowski G, Leduc D, Filee J, Forterre P et al. An alternative flavin-dependent mechanism for thymidylate synthesis. Science 2002; 297:105–107 [View Article] [PubMed]
     [Google Scholar]
  67. Koehn EM, Kohen A. Flavin-dependent thymidylate synthase: a novel pathway towards thymine. Arch Biochem Biophys 2010; 493:96–102 [View Article] [PubMed]
     [Google Scholar]
  68. Pär N, Peter R. Ribonucleotide reductases. Annu Rev Biochem 2006; 75:681–706 [View Article] [PubMed]
     [Google Scholar]
  69. Lundin D, Gribaldo S, Torrents E, Sjöberg B-M, Poole AM. Ribonucleotide reduction - horizontal transfer of a required function spans all three domains. BMC Evol Biol 2010; 10:1–19 [View Article] [PubMed]
     [Google Scholar]
  70. Sakowski EG, Munsell EV, Hyatt M, Kress W, Williamson SJ et al. Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses. Proc Natl Acad Sci U S A 2014; 111:15786–15791 [View Article] [PubMed]
     [Google Scholar]
  71. Wanner Blje, cellular S, biology m. Phosphorus Assimilation and Control of the Phosphate Regulon 1996 pp 1357–1381
     [Google Scholar]
  72. Hsieh YJ, Wanner BL. Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 2010; 13:198–203 [View Article] [PubMed]
     [Google Scholar]
  73. Goldsmith DB, Parsons RJ, Beyene D, Salamon P, Breitbart M. Deep sequencing of the viral phoH gene reveals temporal variation, depth-specific composition, and persistent dominance of the same viral phoH genes in the Sargasso Sea. PeerJ 2015; 3:e997 [View Article] [PubMed]
     [Google Scholar]
  74. Nikkola M, Gleason FK, Eklund H. Reduction of mutant phage T4 glutaredoxins by Escherichia coli thioredoxin reductase. J Biol Chem 1993; 268:3845–3849 [PubMed]
     [Google Scholar]
  75. Gross M, Marianovsky I, Glaser G. MazG -- a regulator of programmed cell death in Escherichia coli. Mol Microbiol 2006; 59:590–601 [View Article] [PubMed]
     [Google Scholar]
  76. LeRoux M, Laub MT. Toxin-antitoxin systems as phage defense elements. Annu Rev Microbiol 2022; 76:21–43 [View Article] [PubMed]
     [Google Scholar]
  77. Rihtman B, Bowman-Grahl S, Millard A, Corrigan RM, Clokie MRJ et al. Cyanophage MazG is a pyrophosphohydrolase but unable to hydrolyse magic spot nucleotides. Environ Microbiol Rep 2019; 11:448–455 [View Article] [PubMed]
     [Google Scholar]
  78. Selje N, Simon M, Brinkhoff TJN. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 2004; 427:445–448 [View Article] [PubMed]
     [Google Scholar]
  79. Voget S, Wemheuer B, Brinkhoff T, Vollmers J, Dietrich S et al. Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J 2015; 9:371–384 [View Article] [PubMed]
     [Google Scholar]
  80. Liu Y, Brinkhoff T, Berger M, Poehlein A, Voget S et al. Metagenome-assembled genomes reveal greatly expanded taxonomic and functional diversification of the abundant marine Roseobacter RCA cluster. Microbiome 2023; 11:265 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001240
Loading
Genome sequences of the first Autographiviridae phages infecting marine Roseobacter
M Gen 10, 001240 (2024); https://doi.org/10.1099/mgen.0.001240
/content/journal/mgen/10.1099/mgen.0.001240
/content/journal/mgen/10.1099/mgen.0.001240
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error