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Volume 105, Issue 3

Forty-nine metagenomic-assembled genomes from an aquatic virome expand by 45 potential new families and the newly uncovered Gossevirus of No Access

Abstract

Twenty complete genomes (29–63 kb) and 29 genomes with an estimated completeness of over 90 % (30–90 kb) were identified for novel dsDNA viruses in the Yangshan Harbor metavirome. These newly discovered viruses contribute to the expansion of viral taxonomy by introducing 46 potential new families. Except for one virus, all others belong to the class . The exception is a novel member of the recently characterized viral group known as Gossevirus. Fifteen viruses were predicted to be temperate. The predicted hosts for the viruses appear to be involved in various aspects of the nitrogen cycle, including nitrogen fixation, oxidation and denitrification. Two viruses were identified to have a host of and , respectively, by matching CRISPR spacers with viral protospacers. Our findings provide an overview for characterizing and identifying specific viruses from Yangshan Harbor. The Gossevirus-like virus uncovered emphasizes the need for further comprehensive isolation and investigation of polinton-like viruses.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacteriophage , Gossevirus , marine environment and metavirome
Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 32370151, 41376135)
    • Principle Award Recipient: YongjieWang
© 2024 The Authors
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/content/journal/jgv/10.1099/jgv.0.001967
2024-03-06
2024-04-27
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References

  1. Weynberg KD. Viruses in marine ecosystems: from open waters to coral reefs. Adv Virus Res 2018; 101:1–38 [View Article] [PubMed]
     [Google Scholar]
  2. Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature 1999; 399:541–548 [View Article] [PubMed]
     [Google Scholar]
  3. Middelboe M, Brussaard CPD. Marine viruses: key players in marine ecosystems. Viruses 2017; 9:302 [View Article] [PubMed]
     [Google Scholar]
  4. Zhang QY, Gui JF. Diversity, evolutionary contribution and ecological roles of aquatic viruses. Sci China Life Sci 2018; 61:1486–1502 [View Article] [PubMed]
     [Google Scholar]
  5. Dion MB, Oechslin F, Moineau S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol 2020; 18:125–138 [View Article] [PubMed]
     [Google Scholar]
  6. Greninger AL. A decade of RNA virus metagenomics is (not) enough. Virus Res 2018; 244:218–229 [View Article] [PubMed]
     [Google Scholar]
  7. Mokili JL, Rohwer F, Dutilh BE. Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2012; 2:63–77 [View Article] [PubMed]
     [Google Scholar]
  8. Batool M, Galloway-Peña J. Clinical metagenomics-challenges and future prospects. Front Microbiol 2023; 14:1186424 [View Article] [PubMed]
     [Google Scholar]
  9. Chen Y, Fan LC, Chai YH, Xu JF. Advantages and challenges of metagenomic sequencing for the diagnosis of pulmonary infectious diseases. Clin Respir J 2022; 16:646–656 [View Article] [PubMed]
     [Google Scholar]
  10. Iuchi H, Kawasaki J, Kubo K, Fukunaga T, Hokao K et al. Bioinformatics approaches for unveiling virus-host interactions. Comput Struct Biotechnol J 2023; 21:1774–1784 [View Article] [PubMed]
     [Google Scholar]
  11. Edwards RA, McNair K, Faust K, Raes J, Dutilh BE. Computational approaches to predict bacteriophage-host relationships. FEMS Microbiol Rev 2016; 40:258–272 [View Article] [PubMed]
     [Google Scholar]
  12. Camargo AP, Nayfach S, Chen IMA, Palaniappan K, Ratner A et al. IMG/VR v4: an expanded database of uncultivated virus genomes within a framework of extensive functional, taxonomic, and ecological metadata. Nucleic Acids Res 2023; 51:D733–D743 [View Article] [PubMed]
     [Google Scholar]
  13. Parthasarathy H, Hill E, MacCallum C. Oceanic metagenomics: global ocean sampling collection. PLoS Biol 2007; 5:0369–0370 [View Article]
     [Google Scholar]
  14. Sunagawa S, Acinas SG, Bork P, Bowler C, Eveillard D et al. Tara oceans: towards global ocean ecosystems biology. Nat Rev Microbiol 2020; 18:428–445 [View Article] [PubMed]
     [Google Scholar]
  15. Wu S, Zhou L, Zhou Y, Wang H, Xiao J et al. Diverse and unique viruses discovered in the surface water of the East China Sea. BMC Genomics 2020; 21:441 [View Article] [PubMed]
     [Google Scholar]
  16. Wang H, Wu S, Li K, Pan Y, Yan S et al. Metagenomic analysis of ssDNA viruses in surface seawater of Yangshan Deep-Water Harbor, Shanghai, China. Marine Genomics 2018; 41:50–53 [View Article]
     [Google Scholar]
  17. Wolf YI, Silas S, Wang Y, Wu S, Bocek M et al. Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome. Nat Microbiol 2020; 5:1262–1270 [View Article] [PubMed]
     [Google Scholar]
  18. Zhou Y, Zhou L, Yan S, Chen L, Krupovic M et al. Diverse viruses of marine archaea discovered using metagenomics. Environ Microbiol 2023; 25:367–382 [View Article] [PubMed]
     [Google Scholar]
  19. Ni Y, Xu T, Yan S, Chen L, Wang Y. Hiding in plain sight: the discovery of complete genomes of 11 hypothetical spindle-shaped viruses that putatively infect mesophilic ammonia-oxidizing archaea. Environ Microbiol Rep 2024; 16:e13230 [View Article]
     [Google Scholar]
  20. Roux S, Hallam SJ, Woyke T, Sullivan MB. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. Elife 2015; 4:e08490 [View Article] [PubMed]
     [Google Scholar]
  21. Bellas CM, Sommaruga R. Polinton-like viruses are abundant in aquatic ecosystems. Microbiome 2021; 9:13 [View Article] [PubMed]
     [Google Scholar]
  22. 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]
  23. 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]
  24. Kieft K, Zhou Z, Anantharaman K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 2020; 8:90 [View Article] [PubMed]
     [Google Scholar]
  25. Ren J, Song K, Deng C, Ahlgren NA, Fuhrman JA et al. Identifying viruses from metagenomic data using deep learning. Quant Biol 2020; 8:64–77 [View Article] [PubMed]
     [Google Scholar]
  26. Nayfach S, Camargo AP, Schulz F, Eloe-Fadrosh E, Roux S et al. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat Biotechnol 2021; 39:578–585 [View Article] [PubMed]
     [Google Scholar]
  27. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article] [PubMed]
     [Google Scholar]
  28. Roux S, Adriaenssens EM, Dutilh BE, Koonin EV, Kropinski AM et al. Minimum Information about an Uncultivated Virus Genome (MIUViG). Nat Biotechnol 2019; 37:29–37 [View Article] [PubMed]
     [Google Scholar]
  29. 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]
  30. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
     [Google Scholar]
  31. Bin Jang H, Bolduc B, Zablocki O, Kuhn JH, Roux S et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol 2019; 37:632–639 [View Article] [PubMed]
     [Google Scholar]
  32. Roux S, Fischer MG, Hackl T, Katz LA, Schulz F et al. Updated virophage taxonomy and distinction from polinton-like viruses. Biomolecules 2023; 13:204 [View Article] [PubMed]
     [Google Scholar]
  33. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article] [PubMed]
     [Google Scholar]
  34. Nishimura Y, Watai H, Honda T, Mihara T, Omae K et al. Environmental viral genomes shed new light on virus-host interactions in the ocean. mSphere 2017; 2:e00359-16 [View Article] [PubMed]
     [Google Scholar]
  35. Bellas C, Hackl T, Plakolb M-S, Koslová A, Fischer MG et al. Large-scale invasion of unicellular eukaryotic genomes by integrating DNA viruses. Proc Natl Acad Sci U S A 2023; 120:e2300465120 [View Article] [PubMed]
     [Google Scholar]
  36. Woo AC, Gaia M, Guglielmini J, Da Cunha V, Forterre P. Phylogeny of the Varidnaviria morphogenesis module: congruence and incongruence with the tree of life and viral taxonomy. Front Microbiol 2021; 12:704052 [View Article] [PubMed]
     [Google Scholar]
  37. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article] [PubMed]
     [Google Scholar]
  38. Oberg N, Zallot R, Gerlt JA. EFI-EST, EFI-GNT, and EFI-CGFP: enzyme function initiative (EFI) web resource for genomic enzymology tools. J Mol Biol 2023; 435:168018 [View Article] [PubMed]
     [Google Scholar]
  39. Tisza MJ, Belford AK, Domínguez-Huerta G, Bolduc B, Buck CB. Cenote-taker 2 democratizes virus discovery and sequence annotation. Virus Evol 2021; 7:veaa100 [View Article] [PubMed]
     [Google Scholar]
  40. Shaffer M, Borton MA, McGivern BB, Zayed AA, La Rosa SL et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res 2020; 48:8883–8900 [View Article]
     [Google Scholar]
  41. Camargo AP, Roux S, Schulz F, Babinski M, Xu Y et al. You can move, but you can’t hide: identification of mobile genetic elements with geNomad. Bioinformatics 2023 [View Article]
     [Google Scholar]
  42. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005; 21:951–960 [View Article] [PubMed]
     [Google Scholar]
  43. Zimmermann L, Stephens A, Nam S-Z, Rau D, Kübler J et al. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol 2018; 430:2237–2243 [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. Gilchrist CLM, Chooi YH. clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 2021; 37:2473–2475 [View Article] [PubMed]
     [Google Scholar]
  46. Darzentas N. Circoletto: visualizing sequence similarity with circos. Bioinformatics 2010; 26:2620–2621 [View Article] [PubMed]
     [Google Scholar]
  47. Burley SK, Bhikadiya C, Bi C, Bittrich S, Chen L et al. RCSB protein data bank: powerful new tools for exploring 3D structures of biological macromolecules for basic and applied research and education in fundamental biology, biomedicine, biotechnology, bioengineering and energy sciences. Nucleic Acids Res 2021; 49:D437–D451 [View Article] [PubMed]
     [Google Scholar]
  48. Holm L, Kääriäinen S, Wilton C, Plewczynski D. Using dali for structural comparison of proteins. Curr Protoc Bio 2006; 5: [View Article] [PubMed]
     [Google Scholar]
  49. Pettersen EF, Goddard TD, Huang CC, Meng EC, Couch GS et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci 2021; 30:70–82 [View Article] [PubMed]
     [Google Scholar]
  50. Chan PP, Lin BY, Mak AJ, Lowe TM. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res 2021; 49:9077–9096 [View Article] [PubMed]
     [Google Scholar]
  51. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S et al. NCBI BLAST: a better web interface. Nucleic Acids Res 2008; 36:W5–W9 [View Article] [PubMed]
     [Google Scholar]
  52. Dion MB, Plante P-L, Zufferey E, Shah SA, Corbeil J et al. Streamlining CRISPR spacer-based bacterial host predictions to decipher the viral dark matter. Nucleic Acids Res 2021; 49:3127–3138 [View Article] [PubMed]
     [Google Scholar]
  53. Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for cas proteins. Nucleic Acids Res 2018; 46:W246–W251 [View Article] [PubMed]
     [Google Scholar]
  54. Roux S, Camargo AP, Coutinho FH, Dabdoub SM, Dutilh BE et al. iPHoP: an integrated machine learning framework to maximize host prediction for metagenome-derived viruses of archaea and bacteria. PLoS Biol 2023; 21:e3002083 [View Article] [PubMed]
     [Google Scholar]
  55. Ghosh D, Chakraborty S, Kodamana H, Chakraborty S. Application of machine learning in understanding plant virus pathogenesis: trends and perspectives on emergence, diagnosis, host-virus interplay and management. Virol J 2022; 19:42 [View Article] [PubMed]
     [Google Scholar]
  56. Sukhorukov G, Khalili M, Gascuel O, Candresse T, Marais-Colombel A et al. VirHunter: a deep learning-based method for detection of novel RNA viruses in plant sequencing data. Front Bioinform 2022; 2:867111 [View Article] [PubMed]
     [Google Scholar]
  57. Johnson G, Banerjee S, Putonti C. Diversity of Pseudomonas aeruginosa temperate phages. mSphere 2022; 7:e0101521 [View Article] [PubMed]
     [Google Scholar]
  58. Li Z, Fang Y, Wang R, Xue J, Chen J. Preliminary study on the DNA-binding properties of phage ΦC31 integrase. Gene 2011; 484:47–51 [View Article] [PubMed]
     [Google Scholar]
  59. Briers Y. Phage Lytic Enzymes. Viruses 2019; 11:113 [View Article] [PubMed]
     [Google Scholar]
  60. Mihara T, Nishimura Y, Shimizu Y, Nishiyama H, Yoshikawa G et al. Linking virus genomes with host taxonomy. Viruses 2016; 8:66 [View Article] [PubMed]
     [Google Scholar]
  61. Low SJ, Džunková M, Chaumeil PA, Parks DH, Hugenholtz P. Evaluation of a concatenated protein phylogeny for classification of tailed double-stranded DNA viruses belonging to the order Caudovirales. Nat Microbiol 2019; 4:1306–1315 [View Article] [PubMed]
     [Google Scholar]
  62. Holm L, Sander C. Dali: a network tool for protein structure comparison. Trends Biochem Sci 1995; 20:478–480 [View Article] [PubMed]
     [Google Scholar]
  63. Krupovic M, Makarova KS, Koonin EV. Cellular homologs of the double jelly-roll major capsid proteins clarify the origins of an ancient virus kingdom. Proc Natl Acad Sci U S A 2022; 119:e2120620119 [View Article] [PubMed]
     [Google Scholar]
  64. Koonin EV, Krupovic M. Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. Curr Opin Virol 2017; 25:7–15 [View Article] [PubMed]
     [Google Scholar]
  65. Chen WM, Huang HW, Chang JS, Han YL, Guo TR et al. Tepidimonas fonticaldi sp. nov., a slightly thermophilic betaproteobacterium isolated from a hot spring. Int J Syst Evol Microbiol 2013; 63:1810–1816 [View Article]
     [Google Scholar]
  66. Lewin GR, Carlos C, Chevrette MG, Horn HA, McDonald BR et al. Evolution and ecology of actinobacteria and their bioenergy applications. Annu Rev Microbiol 2016; 70:235–254 [View Article] [PubMed]
     [Google Scholar]
  67. Zhang B, Wu X, Tai X, Sun L, Wu M et al. Variation in actinobacterial community composition and potential function in different soil ecosystems belonging to the Arid Heihe river basin of Northwest China. Front Microbiol 2019; 10:2209 [View Article] [PubMed]
     [Google Scholar]
  68. Zhu H-Z, Zhang Z-F, Zhou N, Jiang C-Y, Wang B-J et al. Diversity, distribution and co-occurrence patterns of bacterial communities in a Karst Cave system. Front Microbiol 2019; 10:1726 [View Article] [PubMed]
     [Google Scholar]
  69. Seo JH, Kang I, Yang SJ, Cho JC. Characterization of spatial distribution of the bacterial community in the South Sea of Korea. PLoS One 2017; 12:e0174159 [View Article] [PubMed]
     [Google Scholar]
  70. Megrian D, Taib N, Witwinowski J, Beloin C, Gribaldo S. One or two membranes? Diderm firmicutes challenge the Gram-positive/Gram-negative divide. Mol Microbiol 2020; 113:659–671 [View Article] [PubMed]
     [Google Scholar]
  71. Zhao Y, Zhang W, Pan H, Chen J, Cui K et al. Insight into the metabolic potential and ecological function of a novel Magnetotactic Nitrospirota in coral reef habitat. Front Microbiol 2023; 14: [View Article]
     [Google Scholar]
  72. Huang Y, Yang H, Li K, Meng Q, Wang S et al. Red mud conserved compost nitrogen by enhancing nitrogen fixation and inhibiting denitrification revealed via metagenomic analysis. BioRes Technol 2022; 346:126654 [View Article] [PubMed]
     [Google Scholar]
  73. Park S-J, Andrei A-Ş, Bulzu P-A, Kavagutti VS, Ghai R et al. Expanded diversity and metabolic versatility of marine nitrite-oxidizing bacteria revealed by cultivation- and genomics-based approaches. Appl Environ Microbiol 2020; 86:1–17 [View Article] [PubMed]
     [Google Scholar]
  74. Zehr JP, Kudela RM. Nitrogen cycle of the open ocean: from genes to ecosystems. Ann Rev Mar Sci 2011; 3:197–225 [View Article] [PubMed]
     [Google Scholar]
  75. Heyerhoff B, Engelen B, Bunse C. Auxiliary metabolic gene functions in pelagic and benthic viruses of the baltic sea. Front Microbiol 2022; 13:863620 [View Article] [PubMed]
     [Google Scholar]
  76. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU et al. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci U S A 2011; 108:E757–E764 [View Article] [PubMed]
     [Google Scholar]
  77. Luo XQ, Wang P, Li JL, Ahmad M, Duan L et al. Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts. Microbiome 2022; 10:190 [View Article] [PubMed]
     [Google Scholar]
  78. Dremel SE, Jimenez AR, Tucker JM. “Transfer” of power: the intersection of DNA virus infection and tRNA biology. Semin Cell Dev Biol 2023; 146:31–39 [View Article] [PubMed]
     [Google Scholar]
  79. Svedružić ŽM. Dnmt1 structure and function. Prog Mol Biol Transl Sci 2011; 101:221–254 [View Article] [PubMed]
     [Google Scholar]
  80. Lundqvist J, Elmlund D, Heldt D, Deery E, Söderberg CAG et al. The AAA(+) motor complex of subunits CobS and CobT of cobaltochelatase visualized by single particle electron microscopy. J Struct Biol 2009; 167:227–234 [View Article] [PubMed]
     [Google Scholar]
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Forty-nine metagenomic-assembled genomes from an aquatic virome expand Caudoviricetes by 45 potential new families and the newly uncovered Gossevirus of Bamfordvirae
J. Gen. Virol. 105, 001967 (2024); https://doi.org/10.1099/jgv.0.001967
/content/journal/jgv/10.1099/jgv.0.001967
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