Abstract
Microbes drive myriad ecosystem processes, and their viruses modulate microbial-driven processes through mortality, horizontal gene transfer, and metabolic reprogramming by viral-encoded auxiliary metabolic genes (AMGs). However, our knowledge of viral roles in the oceans is primarily limited to surface waters. Here we assess the depth distribution of protein clusters (PCs) in the first large-scale quantitative viral metagenomic data set that spans much of the pelagic depth continuum (the Pacific Ocean Virome; POV). This established ‘core’ (180 PCs; one-third new to science) and ‘flexible’ (423K PCs) community gene sets, including niche-defining genes in the latter (385 and 170 PCs are exclusive and core to the photic and aphotic zones, respectively). Taxonomic annotation suggested that tailed phages are ubiquitous, but not abundant (<5% of PCs) and revealed depth-related taxonomic patterns. Functional annotation, coupled with extensive analyses to document non-viral DNA contamination, uncovered 32 new AMGs (9 core, 20 photic and 3 aphotic) that introduce ways in which viruses manipulate infected host metabolism, and parallel depth-stratified host adaptations (for example, photic zone genes for iron–sulphur cluster modulation for phage production, and aphotic zone genes for high-pressure deep-sea survival). Finally, significant vertical flux of photic zone viruses to the deep sea was detected, which is critical for interpreting depth-related patterns in nature. Beyond the ecological advances outlined here, this catalog of viral core, flexible and niche-defining genes provides a resource for future investigation into the organization, function and evolution of microbial molecular networks to mechanistically understand and model viral roles in the biosphere.
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References
Ackermann HW . (2001). Frequency of morphological phage descriptions in the year 2000. Arch Virol 146: 843–857.
Akashi H, Gojobori T . (2002). Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99: 3695–3700.
Bartlett DH . (2002). Pressure effects on in vivo microbial processes. Biochim Biophys Acta 1595: 367–381.
Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP et al. (2000). Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902–1906.
Bragg JG, Chisholm SW . (2008). Modelling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS One 3: e3550.
Bratbak G . (1993). Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93: 39–48.
Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D et al. (2002). Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99: 14250–14255.
Breitbart M, Felts B, Kelley S, Mahaffy JM, Nulton J, Salamon P et al. (2004). Diversity and population structure of a near-shore marine-sediment viral community. Proc Biol Sci 271: 565–574.
Breitbart M, Thompson LR, Suttle CA, Sullivan MB . (2007). Exploring the vast diversity of marine viruses. Oceanography 20: 135–139.
Breitbart M . (2012). Marine viruses: truth or dare. Ann Rev Mar Sci 4: 425–448.
Brum J . (2005). Concentration, production, and turnover of viruses and dissolved DNA pools at Station ALOHA, North Pacific Subtropical Gyre. Aquat Microb Ecol 41: 103–113.
Brum J, Culley A, Steward G . (2013a). Assembly of a marine viral metagenome after physical fractionation. PLoS ONE 8: e60604.
Brum JR, Steward GF . (2010). Morphological characterization of viruses in the stratified water column of alkaline, hypersaline mono lake. Microb Ecol 60: 636–643.
Brum JR, Schenck RO, Sullivan MB . (2013b). Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J 7: 1738–1751.
Calhoun LN, Kwon YM . (2011). Structure, function and regulation of the DNA-binding protein Dps and its role in acid and oxidative stress resistance in Escherichia coli: a review. J Appl Microbiol 110: 375–386.
Cassman N, Prieto-Davó A, Walsh K, Silva GG, Angly F, Akhter S et al. (2012). Oxygen minimum zones harbour novel viral communities with low diversity. Environ Microbiol 14: 3043–3065.
Clasen J, Elser J . (2007). The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella Virus-1. Freshwater Biol 52: 112–122.
Clokie MRJ, Shan J, Bailey S, Jia Y, Krisch HM . (2006). Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 8: 827–835.
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141–D145.
Colombet J, Sime-Ngando T, Cauchie HM, Fonty G, Hoffmann L, Demeure G . (2006). Depth-related gradients of viral activity in Lake Pavin. Appl Environ Microbiol 72: 4440–4445.
Dammeyer T, Bagby SC, Sullivan MB, Chisholm SW, Frankenberg-Dinkel N . (2008). Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr Biol 18: 442–448.
DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard NU et al. (2006). Community genomics among stratified microbial assemblages in the ocean's interior. Science 311: 496–503.
Deng L, Ignacio-Espinoza JC, Gregory AC, Poulos BT, Weitz JS, Hugenholtz P et al. (2014). Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature ; e-pub ahead of print 13 July 2014 doi:10.1038/nature13459.
Derelle E, Ferraz C, Escande ML, Eychenié S, Cooke R, Piganeau G et al. (2008). Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. PLoS One 3: e2250.
Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM et al. (2008). Functional metagenomic profiling of nine biomes. Nature 452: 629–632.
Duhaime MB, Sullivan MB . (2012). Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology 434: 181–186.
Dwivedi B, Xue B, Lundin D, Edwards RA, Breitbart M . (2013). A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes. BMC Evol Biol 13: 33.
El-Hajj ZW, Tryfona T, Allcock DJ, Hasan F, Lauro FM, Sawyer L et al. (2009). Importance of proteins controlling initiation of DNA replication in the growth of the high-pressure-loving bacterium Photobacterium profundum SS9. J Bacteriol 191: 6383–6393.
Eloe EA, Lauro FM, Vogel RF, Bartlett DH . (2008). The deep-sea bacterium Photobacterium profundum SS9 utilizes separate flagellar systems for swimming and swarming under high-pressure conditions. Appl Environ Microbiol 74: 6298–6305.
Enav H, Mandel-Gutfreund Y, Béjà O . (2014). Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis. Microbiome 2: 1–12.
Falkowski PG, Fenchel T, Delong EF . (2008). The microbial engines that drive Earth's biogeochemical cycles. Science 320: 1034–1039.
Fontecave M, Ollagnier-de-Choudens S . (2008). Iron-sulfur cluster biosynthesis in bacteria: mechanisms of cluster assembly and transfer. Arch Biochem Biophys 474: 226–237.
Frank JA, Lorimer D, Youle M, Witte P, Craig T, Abendroth J et al. (2013). Structure and function of a cyanophage-encoded peptide deformylase. ISME J 7: 1150–1160.
Ghiglione J, Palacios C, Marty J, Mevel G, Labrune C, Conan P et al. (2008). Role of environmental factors for the vertical distribution (0-1000 m) of marine bacterial communities in the NW Mediterranean Sea. Biogeosciences 5: 1751–1764.
Hendrix RW, Lawrence JG, Hatfull GF, Casjens S . (2000). The origins and ongoing evolution of viruses. Trends Microbiol 8: 504–508.
Hengge R . (2008). The two-component network and the general stress sigma factor RpoS (sigma S) in Escherichia coli. Adv Exp Med Biol 631: 40–53.
Henriques AO, Moran CP Jr . (2007). Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 61: 555–588.
Hewson I, Fuhrman JA . (2003). Viriobenthos production and virioplankton sorptive scavenging by suspended sediment particles in coastal and pelagic waters. Microb Ecol 46: 337–347.
Holmfeldt K, Odić D, Sullivan MB, Middelboe M, Riemann L . (2012). Cultivated single-stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA-binding stains. Appl Environ Microbiol 78: 892–894.
Holmfeldt K, Solonenko N, Shah M, Corrier K, Riemann L, Verberkmoes NC et al. (2013). Twelve previously unknown phage genera are ubiquitous in global oceans. Proc Natl Acad Sci USA 110: 12798–12803.
Hopf PS, Ford RS, Zebian N, Merkx-Jacques A, Vijayakumar S, Ratnayake D et al. (2011). Protein glycosylation in Helicobacter pylori: beyond the flagellins? PLoS One 6: e25722.
Huber KE, Waldor MK . (2002). Filamentous phage integration requires the host recombinases XerC and XerD. Nature 417: 656–659.
Hurwitz BL . (2014). TMPL source code. p http://code.google.com/p/tmpl.
Hurwitz BL, Hallam SJ, Sullivan MB . (2013). Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biol 14: R123.
Hurwitz BL, Sullivan MB . (2013). The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One 8: e57355.
Hurwitz BL, Westveld AH, Brum JR, Sullivan MB . (2014). Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses. Proc Natl Acad Sci USA 111: 10714–10719.
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ . (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
Igarashi K, Kashiwagi K . (2010). Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42: 39–51.
Ignacio-Espinoza JC, Sullivan MB . (2012). Phylogenomics of T4 cyanophages: lateral gene transfer in the 'core' and origins of host genes. Environ Microbiol 14: 2113–2126.
Imai R, Ali A, Pramanik HR, Nakaminami K, Sentoku N, Kato H . (2004). A distinctive class of spermidine synthase is involved in chilling response in rice. J Plant Physiol 161: 883–886.
iPlant. (2014). iPlant Collaborative https://www.iplantcollaborative.org/.
Jiang S, Fu W, Chu W, Fuhrman JA . (2003a). The vertical distribution and diversity of marine bacteriophage at a station off Southern California. Microb Ecol 45: 399–410.
Jiang S, Steward G, Jellison R, Chu W, Choi S . (2003b). Abundance, distribution, and diversity of viruses in alkaline, hypersaline Mono Lake, California. Microb Ecol 47: 9–17.
Kanehisa M, Goto S . (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27–30.
Kang I, Oh HM, Kang D, Cho JC . (2013). Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc Natl Acad Sci USA 110: 12343–12348.
Labrie SJ, Frois-Moniz K, Osburne MS, Kelly L, Roggensack SE, Sullivan MB et al. (2012). Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol 155: 1356–1376.
Lang AS, Beatty JT . (2007). Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol 15: 54–62.
Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW . (2004). Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101: 11013–11018.
Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW . (2005). Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86–89.
Mann NH, Cook A, Millard A, Bailey S, Clokie M . (2003). Bacterial photosynthesis genes in a virus. Nature 424: 741.
Millard AD, Zwirglmaier K, Downey MJ, Mann NH, Scanlan DJ . (2009). Comparative genomics of marine cyanomyoviruses reveals the widespread occurrence of Synechococcus host genes localized to a hyperplastic region: implications for mechanisms of cyanophage evolution. Environ Microbiol 11: 2370–2387.
Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R . (2013). Expanding the marine virosphere using metagenomics. PLoS Genet 9: e1003987.
Modi SR, Lee HH, Spina CS, Collins JJ . (2013). Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499: 219–222.
Muda M, Rao NN, Torriani A . (1992). Role of PhoU in phosphate transport and alkaline phosphatase regulation. J Bacteriol 174: 8057–8064.
Ollagnier-de-Choudens S, Sanakis Y, Fontecave M . (2004). SufA/IscA: reactivity studies of a class of scaffold proteins involved in [Fe-S] cluster assembly. J Biol Inorg Chem 9: 828–838.
Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA et al. (2003). Origins of highly mosaic mycobacteriophage genomes. Cell 113: 171–182.
Pitcher RS, Tonkin LM, Daley JM, Palmbos PL, Green AJ, Velting TL et al. (2006). Mycobacteriophage exploit NHEJ to facilitate genome circularization. Mol Cell 23: 743–748.
Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J et al. (2012). eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40: D284–D289.
Qin Q, Li Y, Zhang Y, Zhou Z, Zhang W, Chen X et al. (2011). Comparative genomics reveals a deep-sea sediment-adapted life style of Pseudoalteromonas sp. SM9913. ISME J 5: 274–284.
Rattei T, Arnold R, Tischler P, Lindner D, Stumpflen V, Mewes HW . (2006). SIMAP: the similarity matrix of proteins. Nucleic Acids Res 34: D252.
Rohwer F, Thurber RV . (2009). Viruses manipulate the marine environment. Nature 459: 207–212.
Rouault TA, Tong WH . (2005). Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 6: 345–351.
Rouault TA . (2012). Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis Model Mech 5: 155–164.
Scherzinger E, Lanka E, Hillenbrand G . (1977). Role of bacteriophage T7 DNA primase in the initiation of DNA strand synthesis. Nucleic Acids Res 4: 4151–4163.
Sharon I, Tzahor S, Williamson S, Shmoish M, Man-Aharonovich D, Rusch DB et al. (2007). Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J 1: 492–501.
Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N et al. (2009). Photosystem I gene cassettes are present in marine virus genomes. Nature 461: 258–262.
Sharon I, Battchikova N, Aro EM, Giglione C, Meinnel T, Glaser F et al. (2011). Comparative metagenomics of microbial traits within oceanic viral communities. ISME J 5: 1178–1190.
Shepard EM, Boyd ES, Broderick JB, Peters JW . (2011). Biosynthesis of complex iron-sulfur enzymes. Curr Opin Chem Biol 15: 319–327.
Short CM, Suttle CA . (2005). Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl Environ Microbiol 71: 480.
Solonenko SA, Ignacio-Espinoza JC, Alberti A, Cruaud C, Hallam S, Konstantinidis K et al. (2013). Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 14: 320.
Solonenko SA, Sullivan MB . (2013) Preparation of Metagenomic Libraries from Naturally Occurring Marine Viruses Vol 531 Elsevier: Burlington.
Steward G, Montiel JL, Azam F . (2000). Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol Oceanogr 45: 1697–1706.
Steward GF, Preston CM . (2011). Analysis of a viral metagenomic library from 200 m depth in Monterey Bay, California constructed by direct shotgun cloning. Virol J 8: 287.
Subramanya HS, Doherty AJ, Ashford SR, Wigley DB . (1996). Crystal structure of an ATP-dependent DNA ligase from bacteriophage T7. Cell 85: 607–615.
Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW . (2005). Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3: e144.
Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW . (2006). Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin AM, Kelly L, Weigele PR et al. (2010). Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 12: 3035–3056.
Sun S, Chen J, Li W, Altintas I, Lin A, Peltier S et al. (2011). Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Res 39: D546–D551.
Suttle CA . (2000). Cyanophages and their role in the ecology of cyanobacteria. In Whitton BA, Potts M, (eds) The Ecology of Cyanobacteria. Kluwer Academic Publishers: Netherlands, pp 563–589.
Suttle CA . (2007). Marine viruses—major players in the global ecosystem. Nat Rev Microbiol 5: 801–812.
Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J et al. (2011). Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci USA 108: E757–E764.
Weigele PR, Pope WH, Pedulla ML, Houtz JM, Smith AL, Conway JF et al. (2007). Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 9: 1675–1695.
Wilhelm SW, Weinbauer MG, Suttle CA, Pledger RJ, Mitchell DL . (1998). Measurements of DNA damage and photoreactivation imply that most viruses in marine surface waters are infective. Aq Microb Ecol 14: 215–222.
Williamson SJ, Cary SC, Williamson KE, Helton RR, Bench SR, Winget D et al. (2008). Lysogenic virus-host interactions predominate at deep-sea diffuse-flow hydrothermal vents. ISME J 2: 1112–1121.
Wommack KE, Colwell RR . (2000). Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64: 69–114.
Yonesaki T . (1994). Involvement of a replicative DNA helicase of bacteriophage T4 in DNA recombination. Genetics 138: 247–252.
Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K et al. (2007). The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol 5: e16.
Zeng Q, Chisholm SW . (2012). Marine viruses exploit their host's two-component regulatory system in response to resource limitation. Curr Biol 22: 124–128.
Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC et al. (2013). Abundant SAR11 viruses in the ocean. Nature 494: 357–360.
Acknowledgements
We thank Tucson Marine Phage Lab members for comments on the manuscript; Matt Kane for suggesting the designation of two classes of AMGs; UITS Research Computing Group and the ARL Biotechnology Computing for HPCC access and support. Funding was provided by NSF (DBI-0850105 and OCE-0961947), BIO5 and Gordon and Betty Moore Foundation grants (GBMF2631 and GBMF3790) to MBS, and an NSF Integrative Graduate Education and Research Training Fellowship and NSF Graduate Research Fellowship to BLH.
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Hurwitz, B., Brum, J. & Sullivan, M. Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome. ISME J 9, 472–484 (2015). https://doi.org/10.1038/ismej.2014.143
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DOI: https://doi.org/10.1038/ismej.2014.143
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