Abstract
The species composition and metabolic potential of microbial and viral communities are predictable and stable for most ecosystems. This apparent stability contradicts theoretical models as well as the viral–microbial dynamics observed in simple ecosystems, both of which show Kill-the-Winner behavior causing cycling of the dominant taxa. Microbial and viral metagenomes were obtained from four human-controlled aquatic environments at various time points separated by one day to >1 year. These environments were maintained within narrow geochemical bounds and had characteristic species composition and metabolic potentials at all time points. However, underlying this stability were rapid changes at the fine-grained level of viral genotypes and microbial strains. These results suggest a model wherein functionally redundant microbial and viral taxa are cycling at the level of viral genotypes and virus-sensitive microbial strains. Microbial taxa, viral taxa, and metabolic function persist over time in stable ecosystems and both communities fluctuate in a Kill-the-Winner manner at the level of viral genotypes and microbial strains.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Andersson AF, Banfield JF . (2008). Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320: 1047–1050.
Angly F, Youle M, Nosrat B, Srinagesh S, Rodriguez-Brito B, McNairnie P et al. (2009). Genomic analysis of multiple Roseophage SIO1 strains. Environ Microb 11: 2863–2873.
Angly F, Rodriguez-Brito B, Bangor D, McNairnie P, Breitbart M, Salamon P et al. (2005). PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information. BMC Bioinformatics 6: 41.
Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C et al. (2006). The marine viromes of four oceanic regions. PLoS Biol 4: e368.
Arias CR, Welker TL, Shoemaker CA, Abernathy JW, Klesius PH . (2004). Genetic fingerprinting of Flavobacterium columnare isolates from cultured fish. J Appl Microb 97: 421–428.
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA et al. (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
Benlloch S, Lopez-Lopez A, Casamayor EO, Ovreas L, Goddard V, Daae FL et al. (2002). Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microb 4: 349–360.
Bohannan B, Lenski RE . (2002). Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3: 362–377.
Breitbart M, Rohwer F . (2005). Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. Biotechniques 39: 729–736.
Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P et al. (2003). Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185: 6220–6223.
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, 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.
Briee C, Moreira D, Lopez-Garcia P . (2007). Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microb 158: 213–227.
Bull JJ, Millstein J, Orcutt J, Wichman HA . (2006). Evolutionary feedback mediated through population density, illustrated with viruses in chemostats. Am Nat 167: E39–E51.
Chen F, Wang K, Huang S, Cai H, Zhao M, Jiao N et al. (2009). Diverse and dynamic populations of cyanobacterial podoviruses in the Chesapeake Bay unveiled through DNA polymerase gene sequences. Environ Microbiol 11: 2884–2892.
Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM et al. (2007). The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35: D169–D172.
Cuadros-Orellana S, Martin-Cuadrado A-B, Legault BA, D’Auria G, Zhaxybayeva O, Papke RT et al. (2007). Genomic plasticity in prokaryotes: the case of the square haloarchaeon. ISME J 1: 235–245.
DeSantis TZ, Dubosarskiy I, Murray SR, Andersen GL . (2003). Comprehensive aligned sequence construction for automated design of effective probes (CASCADE-P) using 16S rDNA. Bioinformatics 19: 1461–1468.
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al. (2006). Greengenes: a chimera-checked 16S rRNA gene database and workbench compatible with ARB. App Environ Microb 72: 5069–5072.
Desnues C, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T, Haynes M et al. (2008). Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452: 340–343.
Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L et al. (2008a). Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 3: e1584.
Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM et al. (2008b). Functional metagenomic profiling of nine biomes. Nature 452: 629–632.
Edwards RA, Rohwer F . (2005). Viral metagenomics. Nat Rev Microb 3: 504–510.
Edwards RA, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson DM et al. (2006). Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7: 57.
Fredslund J . (2006). Phi-Fi: fast and easy online creation and manipulation of phylogeny color figures. BMC Bioinformatics 7: 315.
Fuhrman JA, Schwalbach MS . (2003). Viral influence on aquatic bacterial communities. Biol Bull 204: 192–195.
Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown V, Naeem S . (2006). Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103: 13104–13109.
Garland JL, Mills AL . (1991). Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. App Environ Microb 57: 2351–2359.
Harcombe WR, Bull JJ . (2005). Impact of phages on two-species bacterial communities. App Environ Microb 71: 5254–5259.
Hoffmann KH, Rodriguez-Brito B, Breitbart M, Bangor D, Angly F, Felts B et al. (2007). Power law rank-abundance models for marine phage communities. FEMS Microb Lett 273: 224–228.
Holmfeldt K, Middelboe M, Nybroe O, Riemann L . (2007). Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their flavobacterium hosts. App Environ Microb 73: 6730–6739.
Horner-Devine MC, Lage M, Hughes JB, Bohannan B . (2004). A taxa-area relationship for bacteria. Nature 432: 750–753.
Huson DH, Auch AF, Qi J, Schuster SC . (2007). MEGAN analysis of metagenomic data. Genome Res 17: 377–386.
Kunin V, He S, Warnecke F, Peterson SB, Garcia Martin H, Haynes M et al. (2008). A bacterial metapopulation adapts locally to phage predation despite global dispersal. Genome Res 18: 293–297.
Legault BA, Lopez-Lopez A, Alba-Casado JC, Doolittle WF, Bolhuis H, Rodriguez-Valera F et al. (2006). Environmental genomics of ‘Haloquadratum walbyi’ in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genomics 7: 171.
Lennon JT, Martiny JBH . (2008). Rapid evolution buffers ecosystem impacts of viruses in a microbial food web. Ecol Lett 11: 1178–1188.
Lindstrom ES, Kamst-Van Agterveld MP, Zwart G . (2005). Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microb 71: 8201–8206.
Liu M, Deora R, Doulatov SR, Gingery M, Eiserling FA, Preston A et al. (2002). Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295: 2091–2094.
Lozupone C, Knight R . (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228–8235.
Lozupone C, Hamady M, Knight R . (2006). UniFrac--an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7: 371.
Middelboe M . (2000). Bacterial growth rate and marine virus-host dynamics. Microb Ecol 40: 114–124.
Middelboe M, Holmfeldt K, Riemann L, Nybroe O, Haaber J . (2009). Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environ Microb 11: 1971–1982.
Middelboe M, Hagstrom A, Blackburn N, Sinn B, Fischer U, Borch NH et al. (2001). Effects of bacteriophages on the population dynamics of four strains of pelagic marine bacteria. Microb Ecol 42: 395–406.
Noble RT, Fuhrman JA . (1997). Virus decay and its causes in coastal waters. Appl Environ Microb 63: 77–83.
Noble RT, Fuhrman JA . (1998). Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113–118.
Noble RT, Fuhrman JA . (2000). Rapid virus production and removal as measured with fluorescently labeled viruses as tracers. Appl Environ Microb 66: 3790–3797.
Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M et al. (2005). The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33: 5691–5702.
Parkinson N, Stead D, Bew J, Heeney J, Tsror LL, Elphinstone J . (2009). Dickeya species relatedness and clade structure determined by comparison of recA sequences. Int J Syst Evol Microbiol 59: 2388–2393.
Pasic L, Rodriguez-Mueller B, Martin-Cuadrado A-B, Mira A, Rohwer F, Rodriguez-Valera F . (2009). Metagenomic islands of hyperhalophiles: the case of Salinibacter ruber. BMC Genomics 10: 570–580.
Rodriguez-Brito B, Rohwer F, Edwards RA . (2006). An application of statistics to comparative metagenomics. BMC Bioinformatics 7: 162.
Rodriguez-Valera F, Ventosa A, Juez G, Imhoff JF . (1985). Variation of environmental features and microbial populations with salt concentrations in a multi-pond saltern. Microb Ecol 11: 107–115.
Rodriguez-Valera F, Martin-Cuadrado A-B, Rodriguez-Brito B, Pašić L, Thingstad TF, Rohwer F et al. (2009). Explaining microbial population genomics through phage predation. Nat Rev Microbiol 7: 828–836.
Rohwer F, Edwards R . (2002). The Phage Proteomic Tree: a genome-based taxonomy for phage. J Bacteriol 184: 4529–4535.
Sambrook J, Fritsch EF, Maniatis T . (1982). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York, USA.
Short SM, Short CM . (2009). Quantitative PCR reveals transient and persistent algal viruses in Lake Ontario, Canada. Environ Microbiol 11: 2639–2648.
Sigee DC . (2005). Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the freshwater environment. In: Sigee DC (ed). Freshwater Microbiology. John Wiley & Sons, Ltd.: England, pp 105–180.
Stoddard LI, Martiny JBH, Marston MF . (2007). Selection and characterization of cyanophage resistance in marine Synechococcus strains. App Environ Microb 73: 5516–5522.
Taylor R . (1984). Predation Chapman & Hall: New York, New York, USA.
Thingstad F . (1997). A theoretical approach to structuring mechanisms in the pelagic food web. Hydrobiologia 363: 59–72.
Thingstad F . (2000). Elements of a theory for the mechanisms controlling abundance, diversity and the biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45: 1320–1328.
Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW et al. (2005). Comparative metagenomics of microbial communities. Science 308: 554–557.
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI . (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027–1031.
Tyson GW, Banfield JF . (2008). Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microb 10: 200–207.
Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM et al. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37–43.
Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66–74.
Vos M, Birkett PJ, Birch E, Griffiths RI, Buckling A . (2009). Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325: 833.
Whitman WB, Coleman DC, Wiebe WJ . (1998). Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95: 6578–6583.
Willner D, Thurber RV, Rohwer F . (2009). Metagenomic signatures of 86 microbial and viral metagenomes. Environ Microb 11: 1752–1766.
Winget DM, Wommack KE . (2009). Diel and daily fluctuations in virioplankton production in coastal ecosystems. Environ Microbiol 11: 2904–2914.
Wommack KE, Ravel J, Hill RT, Chun J, Colwell RR . (1999). Population dynamics of Chesapeake Bay virioplankton: total-community analysis by pulsed-field gel electrophoresis. App Environ Microb 65: 231–240.
Yannarell AC, Triplett EW . (2005). Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microb 71: 227–239.
Zehr JP, Jenkins BD, Short SM, Steward GF . (2003). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microb 5: 539–554.
Zhong Y, Chen F, Wilhelm SW, Poorvin L, Hodson RE . (2002). Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20. App Environ Microb 68: 1576–1584.
Zhou J, Spratt BG . (1992). Sequence diversity within the argF, fbp and recA genes of natural isolates of Neisseria meningitidis: interspecies recombination within the argF gene. Mol Microbiol 6: 2135–2146.
Acknowledgements
We thank the Chula Vista Saltern Works and Kent Sea Tech for all their invaluable help and collaboration during this study. Funding for this study was received from the US National Science Foundation (DEB-BE04-21955), Gordon and Betty Moore Foundation, ARCS Fellowship, NSF Postdoctoral Fellowship #DBI-0511948, ATP/Kent Sea Tech and EMBO ASTF366-2007 short-term fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Rodriguez-Brito, B., Li, L., Wegley, L. et al. Viral and microbial community dynamics in four aquatic environments. ISME J 4, 739–751 (2010). https://doi.org/10.1038/ismej.2010.1
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2010.1
Keywords
This article is cited by
-
Virome Analysis of Paddy Floodwater in Two Cropping Seasons
Indian Journal of Microbiology (2024)
-
Serratia marcescens in the intestine of housefly larvae inhibits host growth by interfering with gut microbiota
Parasites & Vectors (2023)
-
Genome analysis of haloalkaline isolates from the soda saline crater lake of Isabel Island; comparative genomics and potential metabolic analysis within the genus Halomonas
BMC Genomics (2023)
-
Viruses under the Antarctic Ice Shelf are active and potentially involved in global nutrient cycles
Nature Communications (2023)
-
Metagenomic analysis of heavy metal-contaminated soils reveals distinct clades with adaptive features
International Journal of Environmental Science and Technology (2023)
