Abstract
Microbial oceanography is an emerging discipline resulted from the interaction, cross-fertilization and integration of life science and ocean science. Microbial oceanography integrates the principles of marine microbiology, microbial ecology and oceanography to study the role of microorganisms in the biogeochemical dynamics of natural marine ecosystems. The application of genomics tools to study marine microbes is resulting in rapid advancements in microbial oceanography that has important implications in global carbon cycle, climate change, and ecosystem function. Here we review the application of genomics and metagenomics in microbial oceanography and suggest future directions in microbial oceanography research.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Karl D M. Microbial oceanography: Paradigms, processes and promise. Nature Rev Microbiol, 2007, 5: 759–769
Karl D M, Proctor L M. Foundations of microbial oceanography. Oceanography, 2007, 16: 16–27
Hallam S J, Mincer T J, Schleper C, et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine crenarchaeota. PLoS Biol, 2006, 4: 0520–0536
Doolittle W F, Papke R T. Genomics and the bacterial species problem. Genome Biol, 2006, 7: 116
Venter J C, Remington K, Heidelberg J F, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science, 2004, 304: 66–74
Pomeroy L R, Williams P J, Azam F, et al. The microbial loop. Oceanography, 2007, 20: 28–33
Ducklow H W, Steinberg D K, Buesseler K O. Upper ocean carbon export and the biological pump. Oceanography, 2001, 14: 50–58
Jiao N, Herndl G, Hansell D A, et al. Microbial production of recalcitrant dissolved organic matter: Long-term carbon storage in the global ocean. Nat Rev Microbiol, 2010, 8: 593–599
Breitbart M, Thompson L R, Suttle C A, et al. Exploring the vast diversity of marine virus. Oceanography, 2007, 20: 135–139
Rohwer F, Thurber R V. Marine viruses: Manipulating the marine environment. Nature, 2009, 459: 207–212
Dickey T D. The emergence of concurrent high-resolution physical and bio-optical measurements in the upper ocean and their applications. Rev Geophys, 1991, 29: 383–413
Helmreich S. Alien Ocean: Anthropological Voyages in Microbial Seas. Berkeley: University of California Press, 2009. 464
Karl D M, Letelier R. Marine habitats and conditions for microbial growth. In: Schaechter M, ed. Encyclopedia of Microbiology. 3rd ed. Oxford: Elsevier, 2009. 258–277
Chisholm S W. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature, 1988, 334: 340–343
Azam F, Malfatti F. Microbial structuring of marine ecosystems. Nat Rev Microbiol, 2007, 5: 782–791
Herndl G J, Reinthaler T. The TRANSAT & ARCHIMEDES Shipboard Parties. Potential of Microbial Oceanography to Shed Light on the Dark Ocean’s Enigmas. NIOZ Annual Report, 2008. http://www.nioz.nl/public/annual_report/2008/herndl.pdf
Whitman W B, Coleman D C, Wiebe W J, et al. Prokaryotes: The unseen majority. Proc Natl Acad Sci USA, 1998, 95: 6578–6583
Doney S, Abbott M, Cullen J, et al. From genes to ecosystems: The ocean’s new frontier. Front Ecol Environ, 2004, 2: 457–466
Aristegui J, Gasol J M, Duarte C M, et al. Microbial oceanography of the dark ocean’s pelagic realm. Limn Oceanogr, 2009, 54: 1501–1529
Lauro F M, Chastain R A, Blankenship L E, et al. The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl Environ Microbiol, 2007, 73: 838–845
Falkowski P, Scholes R J, Boyle E, et al. The global carbon cycle: A test of our knowledge of Earth as a system. Science, 2000, 290: 291–296
Bowler C, Karl D, Colwell R. Microbial oceanography in a sea of opportunity. Nature, 2009, 459: 180–184
Schlesinger W H. Biogeochemistry: An Analysis of Global Change. London: Academic Press, 1997. 588
Strom S L. Microbial ecology of ocean biogeochemistry: A community perspective. Science, 2008, 320: 1043–1045
Cullen J J, Doolittle W F, Levin S A, et al. Patterns and prediction in microbial oceanography. Oceanography, 2007, 20: 34–46
Fuhrman J A. Microbial community structure and its functional implications. Nature, 2009, 459: 193–199
Sogin M L, Morrison H G, Huber J A, et al. Micrboial diversity in the deep sea and the underexplored “rare biosphere.” Proc Natl Acad Sci USA, 2006, 103: 12115–12120
Fang J, Zhang L, Bazylinski D A. Deep-sea piezosphere and piezophiles: Geomicrobiology and biogeochemistry. Trends Microbiol, 2010, 18: 413–422
Amann R I, Ludwig W, Schleifer K H, et al. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev, 1995, 59: 143–169
Rappe M S, Giovannoni S J. The uncultured microbial majority. Annu Rev Microbiol, 2003, 57: 369–394
Pace N R. A molecular view of microbial diversity and the biosphere. Science, 1997, 276: 734–740
Giovannoni S, Stingl U. The importance of culturing bacterioplankton in the ‘omics’ age. Nature Rev Microbiol, 2007, 5: 820–826
DeLong E F. Archaea in coastal marine environments. Proc Natl Acad Sci USA, 1992, 89: 5685–5689
Fuhrman J A, McCallum K, Davis A A. Novel major archaebacterial group from marine plankton. Nature, 1992, 356: 148–149
Massana R, Murray A E, Preston C M, et al. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara channel. Appl Environ Microbiol, 1997, 63: 50–56
Karner M B, DeLong E F, Karl D M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature, 2001, 409: 507–510
Herndl G J, Reinthaler T, Teira E, et al. Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol, 2005, 71: 2303–2309
Pearson A, McNichol A P, Benitez-Nelson B C, et al. Origins of lipid biomarkers in Santa Monica Basin surface sediment: A case study using compound-specific 14C analysis. Geochim Cosmochim Acta, 2001, 65: 3123–3137
Könneke M, Bernhard A E, de la Torre J R, et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 2005, 437: 543–546
Hallam S J, Konstantinidis K T, Putnam N, et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA, 2006, 103: 18296–18301
Mincer T J, Church M J, Taylor L T, et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol, 2007, 9: 1162–1175
Francis C A, Beman J M, Kuypersl M M M. New processes and players in the nitrogen cycle: The microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J, 2007, 1: 19–27
DeLong E F. The microbial ocean from genomes to biomes. Nature, 2009, 459: 200–206
Venter J C, Remington K, Heidelberg J F, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science, 2004, 304: 66–74
Tringe S G, Von Mering C, Kobayashi A, et al. Comparative metagenomics of microbial communities. Science, 2005, 308: 554–557
Tringe S G, Rubin E M. Metagenomics: DNA sequencing of environmental samples. Nature Rev Genetics, 2005, 6: 805–814
Mou X, Sun S, Edwards R A, et al. Bacterial carbon processing by generalist species in the coastal ocean. Nature, 2008, 451: 708–714
Kerkhof L J, Goodman R M. Ocean microbial metagenomics. Deep-Sea Res II, 2009, 56: 1824–1829
Medini D, Serruto D, Parkhil J, et al. Microbiology in the post-genomic era. Nature Rev Microbiol, 2008, 6: 1–13
Béjà O, Aravind L, Koonin E V, et al. Bacterial rhodopsin: Evidence for a new type of phototrophy in the sea. Science, 2000, 289: 1902–1906
Giovannoni S J, Bibbs L, Cho J C, et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature, 2005, 438: 82–85
Gómez-Consarnau L, González J M, Coll-Lladó M, et al. Light stimulates growth of proteorhodopsin-containing marine flavobacteria. Nature, 2007, 445: 210–213
Tripp H J, Bench S R, Turk K A, et al. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature, 2010, 464: 90–94
Jiao N Z, Zhang Y, Zeng Y, et al. Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ Microbiol, 2007, 9: 3091–3099
Jiao N, Zhang F, Hong N. Significant roles of bacteriochlorophylla supplemental to chlorophylla in the ocean. ISME J, 2009, 4: 595–597
Cottrell M T, Ras J, Kirchman D L. Bacteriochlorophyll and community structure of aerobic anoxygenic phototrophic bacteria in a particle-rich estuary. ISME J, 2010, 4: 945–954
DeLong E F, Preston C M, Mincer T, et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science, 2006, 311: 496–503
Martin-Cuadrado A B, López-García P, Alba J C, et al. Metagenomics of the deep Mediterranean, a warm bathypelagic habitat. PLoS ONE, 2007, 2: e914
Fang J, Zhang L. Explore the deep biosphere. Sci China-Earth Sci, 2011, 54: 157–165
National Research Council. The New Science of Metagenomics: Revealing the Secrets of Our Microbial Planet. Washington DC: The National Academies Press, 2008. 170
Helmreich S. Alien Ocean: Anthropological Voyages in Microbial Seas. Berkeley: University of California Press, 2009. 464
Tyson G W, Chapman J, Hugenholtz P, et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature, 2004, 428: 37–43
DeLong E F, Karl D M. Genomic perspectives in microbial oceanography. Nature, 2005, 437: 336–342
Frias-Lopez J, Shi Y, Tyson G W, et al. Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA, 2008, 105: 3805–3810
Ingalls A E, Shah S R, Hansman R L, et al. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci USA, 2006, 103: 6442–6447
Neufeld J D, Wagner M, Murrell J C. Who eats what, where and when? Isotopelabelling experiments are coming of age. ISME J, 2007, 1: 103–110
Shi Y, Tyson G W, DeLong E F. Metatranscriptomics reveals unique microbial small RNAs in the ocean’s water column. Nature, 2009, 459: 266–269
Stingl U, Tripp H J, Giovannoni S J. Improvements of highthroughput 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
Zengler K, Toledo G, Rappé M, et al. Cultivating the uncultured. Proc Natl Acad Sci USA, 2002, 99: 15681–15686
Takai K, Miyazaki M, Hirayama H, et al. Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ Microbiol, 2009, 11: 1983–1997
Kaeberlein T, Lewis K, Epstein S S. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science, 2002, 296: 1127–1129
Ferrari B C, Binnerup S J, Gillings M, et al. Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Appl Environ Microbiol, 2005, 71: 8714–8720
Park H S, Schumacher R, Kilbane J J. New method to characterize microbial diversity using flow cytometry. J Ind Microbiol Biotechnol, 2005, 32: 94–102
Lasken R S, Kvist T, Ishøy T, et al. Multiple Displacement Amplification from single bacterial cells. In: Hughes S, Lasken R, eds. Whole Genome Amplification. Banbury: Scion Publishing Ltd., 2005. 119–147
Lasken R S. Single-cell genomic sequencing using multiple displacement amplification. Curr Opin Microbiol, 2007, 10: 510–516
Walker A, Parkhill J. Single-cell genomics. Nat Rev Microbiol, 2008, 6: 176–177
Siegl A, Kamke J, Hochmuth T, et al. Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J, 2011, 5: 61–70
Woyke T, Tighe D, Mavromatis K, et al. One bacterial cell, one complete genome. PLoS ONE 2010, 5: e10314, doi: 10.1371/journal.pone.0010314
Seshadri R, Kravitz S A, Smarr L, et al. CAMERA: A community resource for metagenomics. PLoS Biol, 2007, 5: e75
Rothstein L, Cullen J, Abbott M, et al. Modeling ocean ecosystem: The PARADIGM program. Oceanography, 2006, 19: 22–51
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fang, J., Zhang, L. Genomics, metagenomics, and microbial oceanography—A sea of opportunities. Sci. China Earth Sci. 54, 473–480 (2011). https://doi.org/10.1007/s11430-011-4179-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11430-011-4179-0