Abstract
Vertical, seasonal and geographical patterns in ocean microbial communities have been observed in many studies, but the resolution of community dynamics has been limited by the scope of data sets, which are seldom up to the task of illuminating the highly structured and rhythmic patterns of change found in ocean ecosystems. We studied vertical and temporal patterns in the microbial community composition in a set of 412 samples collected from the upper 300 m of the water column in the northwestern Sargasso Sea, on cruises between 1991 and 2004. The region sampled spans the extent of deep winter mixing and the transition between the euphotic and the upper mesopelagic zones, where most carbon fixation and reoxidation occurs. A bioinformatic pipeline was developed to de-noise, normalize and align terminal restriction fragment length polymorphism (T-RFLP) data from three restriction enzymes and link T-RFLP peaks to microbial clades. Non-metric multidimensional scaling statistics resolved three microbial communities with distinctive composition during seasonal stratification: a surface community in the region of lowest nutrients, a deep chlorophyll maximum community and an upper mesopelagic community. A fourth microbial community was associated with annual spring blooms of eukaryotic phytoplankton that occur in the northwestern Sargasso Sea as a consequence of winter convective mixing that entrains nutrients to the surface. Many bacterial clades bloomed in seasonal patterns that shifted with the progression of stratification. These richly detailed patterns of community change suggest that highly specialized adaptations and interactions govern the success of microbial populations in the oligotrophic ocean.
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References
Azam F, Long RA . (2001). Oceanography—sea snow microcosms. Nature 414: 495–498.
Azam F, Malfatti F . (2007). Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782–791.
Bano N, Hollibaugh JT . (2002). Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl Environ Microbiol 68: 505–518.
Béjà O, Aravind L, Koonin EV, Suzuki M, Hadd A, Nguyen LP et al. (2000a). Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902–1906.
Béjà O, Suzuki MT, Koonin EV, Aravind L, Hadd A, Nguyen LP et al. (2000b). Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ Microbiol 2: 516–529.
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL . (2008). GenBank. Nucleic Acids Res 36: D25–D30.
Brown MV, Donachie SP . (2007). Evidence for tropical endemicity in the Deltaproteobacteria Marine Group B/SAR324 bacterioplankton clade. Aquatic Microbial Ecology 46: 107–115.
Burton RM, Treusch AH, Finlay LA, Donatz M, Giovannoni SJ . (2009). BestBet. http://www.mcb.oregonstate.edu/giovannoni/.
Carlson CA, Ducklow HW . (1996). Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat Microb Ecol 10: 69–85.
Carlson CA, Ducklow HW, Michaels AF . (1994). Annual flux of dissolved organic carbon from the euphotic zone in the northwestern Sargasso Sea. Nature 371: 405–408.
Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K . (2009). Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J 3: 283–295.
Clarke KR . (1993). Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117–143.
Cohan FM . (2006). Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philos Trans R Soc Lond B Biol Sci 361: 1985–1996.
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.
DeLong EF, Taylor LT, Marsh TL, Preston CM . (1999). Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl Environ Microbiol 65: 5554–5563.
Dortch Q, Roberts TL, Clayton JR, Ahmed SI . (1983). RNA DNA ratios and DNA concentrations as indicators of growth-rate and biomass in planktonic marine organisms. Mar Ecol Prog Ser 13: 61–71.
Ducklow HW, Doney SC, Steinberg DK . (2009). Contributions of long-term research and time-series observations to marine ecology and biogeochemistry. Annu Rev Mar Sci 1: 279–302.
Durand MD, Olson RJ, Chisholm SW . (2001). Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep Sea Res Part II Top Stud Oceanogr 48: 1983–2003.
Egert M, Friedrich MW . (2005). Post-amplification Klenow fragment treatment alleviates PCR bias caused by partially single-stranded amplicons. J Microbiol Methods 61: 69–75.
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P . (1998). Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237–240.
Finlay LA, Burton RM, Kujawinski EB, Giovannoni SJ . (2009). T-RFLP-adjust. http://www.mcb.oregonstate.edu/giovannoni/.
Fuhrman JA, Davis AA . (1997). Widespread Archaea and novel bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar Ecol Prog Ser 150: 275–285.
Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S . (2006). Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103: 13104–13109.
Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL et al. (2008). A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA 105: 7774–7778.
Gin KYH, Chisholm SW, Olson RJ . (1999). Seasonal and depth variation in microbial size spectra at the Bermuda Atlantic time series station. Deep Sea Res Part I Oceanogr Res Pap 46: 1221–1245.
Giovannoni S, Rappé M, Vergin K, Adair N . (1996). 16S rRNA genes reveal stratified open ocean bacterioplankton populations related to the Green Non-Sulfur bacteria. Proc Natl Acad Sci USA 93: 7979–7984.
Giovannoni SJ, Bibbs L, Cho JC, Stapels MD, Desiderio R, Vergin KL et al. (2005a). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438: 82–85.
Giovannoni SJ, Hayakawa DH, Tripp HJ, Stingl U, Givan SA, Cho JC et al. (2008). The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10: 1771–1782.
Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin K, Batista D et al. (2005b). Genome streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242–1245.
Gonzalez JM, Simo R, Massana R, Covert JS, Casamayor EO, Pedros-Alio C et al. (2000). Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl Environ Microbiol 66: 4237–4246.
Gordon DA, Giovannoni SJ . (1996). Stratified microbial populations related to Chlorobium and Fibrobacter detected in the Atlantic and Pacific Oceans. Appl Environ Microbiol 62: 1171–1177.
Hansell DA, Carlson CA . (2001). Biogeochemistry of total organic carbon and nitrogen in the Sargasso Sea: control by convective overturn. Deep Sea Res Part II Top Stud Oceanogr 48: 1649–1667.
Hewson I, Steele JA, Capone DG, Fuhrman JA . (2006). Remarkable heterogeneity in meso- and bathypelagic bacterioplankton assemblage composition. Limnol Oceanogr 51: 1274–1283.
Heywood JL, Zubkov MV, Tarran GA, Fuchs BM, Holligan PM . (2006). Prokaryoplankton standing stocks in oligotrophic gyre and equatorial provinces of the Atlantic Ocean: Evaluation of inter-annual variability. Deep Sea Res Part II Top Stud Oceanogr 53: 1530–1547.
Hunt DE, David LA, Gevers D, Preheim SP, Alm EJ, Polz MF . (2008). Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320: 1081–1085.
Kaplan CW, Kitts CL . (2003). Variation between observed and true terminal restriction fragment length is dependent on true TRF length and purine content. J Microbiol Methods 54: 121–125.
Karner MB, DeLong EF, Karl DM . (2001). Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507–510.
Kemp PF, Lee S, LaRoche J . (1993). Estimating the growth rate of slowly growing marine bacteria from RNA content. Appl Environ Microbiol 59: 2594–2601.
Kent AD, Smith DJ, Benson BJ, Triplett EW . (2003). Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl Environ Microbiol 69: 6768–6776.
Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, Ward DM et al. (2008). Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci USA 105: 2504–2509.
Liu WT, Marsh TL, Cheng H, Forney LJ . (1997). Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516–4522.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363–1371.
Marsh TL, Saxman P, Cole J, Tiedje J . (2000). Terminal restriction fragment length polymorphism analysis program, a web-based research tool for microbial community analysis. Appl Environ Microbiol 66: 3616–3620.
McCune B, Grace JB . (2002). Analysis of ecological communities. MJM Software.
Michaels AF, Olson D, Sarmiento JL, Ammerman JW, Fanning K, Jahnke R et al. (1996). Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. Biogeochemistry 35: 181–226.
Moeseneder MM, Arrieta JM, Muyzer G, Winter C, Herndl GJ . (1999). Optimization of terminal-restriction fragment length polymorphism analysis for complex marine bacterioplankton communities and comparison with denaturing gradient gel electrophoresis. Appl Environ Microbiol 65: 3518–3525.
Moore LR, Rocap G, Chisholm SW . (1998). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467.
Morris RM, Cho JC, Rappé MS, Vergin KL, Carlson CA, Giovannoni SJ . (2005). Bacterioplankton responses to deep seasonal mixing in the Sargasso Sea. Limnol Oceanogr 50: 382–391.
Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA et al. (2002). SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806–810.
Morris RM, Rappe MS, Urbach E, Connon SA, Giovannoni SJ . (2004). Prevalence of the Chloroflexi-related SAR202 bacterioplankton cluster throughout the mesopelagic zone and deep ocean. Appl Environ Microbiol 70: 2836–2842.
Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K et al. (1998). Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64: 2585–2595.
Murray AE, Wu KY, Moyer CL, Karl DM, DeLong EF . (1999). Evidence for circumpolar distribution of planktonic Archaea in the Southern Ocean. Aquat Microb Ecol 18: 263–273.
Nelson DM, Brzezinski MA . (1997). Diatom growth and productivity in an oligotrophic midocean gyre: A 3-yr record from the Sargasso Sea near Bermuda. Limnol Oceanogr 42: 473–486.
Nelson JD, Boehme SE, Reimers CE, Sherrell RM, Kerkhof LJ . (2008). Temporal patterns of microbial community structure in the Mid-Atlantic Bight. FEMS Microbiol Ecol 65: 484–493.
Nocker A, Burr M, Camper AK . (2007). Genotypic microbial community profiling: a critical technical review. Microb Ecol 54: 276–289.
Olson RJ, Chisholm SW, Zettler ER, Altabet MA, Dusenberry JA . (1990a). Spatial and temporal distributions of prochlorophyte picoplankton in the North-Atlantic Ocean. Deep Sea Res Part a Oceanogr Res Pap 37: 1033–1051.
Olson RJ, Chisholm SW, Zettler ER, Armburst EV . (1990b). Pigments, size, and distribution of Synechococcus in the North Atlantic and Pacific Oceans. Limnol Oceanogr 35: 45–58.
Osborne CA, Rees GN, Bernstein Y, Janssen PH . (2006). New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl Environ Microbiol 72: 1270–1278.
Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P et al. (2007). Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16: 867–880.
Reinthaler T, van Aken H, Veth C, Aristegui J, Robinson C, Williams PJLR et al. (2006). Prokaryotic respiration and production in the meso- and bathypelagic realm of the eastern and western North Atlantic basin. Limnol Oceanog 51: 1262–1273.
Reysenbach A-L, Giver LJ, Wickham GS, Pace NR . (1992). Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58: 3417–3418.
Ricke P, Kolb S, Braker G . (2005). Application of a newly developed ARB software-integrated tool for in silico terminal restriction fragment length polymorphism analysis reveals the dominance of a novel pmoA cluster in a forest soil. Appl Environ Microbiol 71: 1671–1673.
Schlitzer R . (2000). Ocean Data View. http://www.awi-bremerhaven.de/GEO/ODV.
Sprintall J, Tomczak M . (1992). Evidence of the barrier layer in the surface-layer of the Tropics. J Geophys Res Oceans 97: 7305–7316.
Steinberg DK, Carlson CA, Bates NR, Johnson RH, Michaels AF, Knap AH . (2001). Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biochemistry. Deep Sea Res II 48: 1405–1447.
Suzuki MT, Beja O, Taylor LT, Delong EF . (2001). Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ Microbiol 3: 323–331.
Suzuki MT, Preston CM, Beja O, de la Torre JR, Steward GF, DeLong EF . (2004). Phylogenetic screening of ribosomal RNA gene-containing clones in Bacterial Artificial Chromosome (BAC) libraries from different depths in Monterey Bay. Microb Ecol 48: 473–488.
Varela MM, van Aken HM, Herndl GJ . (2008). Abundance and activity of Chloroflexi-type SAR202 bacterioplankton in the meso- and bathypelagic waters of the (sub) tropical Atlantic. Environ Microbiol 10: 1903–1911.
Vergin KL, Rappe MS, Giovannoni SJ . (2001). Streamlined method to analyze 16S rRNA gene clone libraries. Biotechniques 30: 938–940, 943–934.
Wright TD, Vergin KL, Boyd PW, Giovannoni SJ . (1997). A novel delta-subdivision proteobacterial lineage from the lower ocean surface layer. Appl Environ Microbiol 63: 1441–1448.
Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P et al. (2006). Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103: 12317–12322.
Acknowledgements
We thank the officers and crew of the RV Weatherbird II for their assistance and support and the BATS chief scientists and technicians for assistance in water collection and accommodating wire time requests. We thank Rachel Parsons for technical assistance and Robert Morris for his constructive input. This research was funded by a grant from the Marine Microbiology Initiative of the Gordon and Betty Moore Foundation to SJG and NSF Microbial Observatory grants MCB-0237728 & OCE-0801991 to CAC and SJG. AHT is supported by a Feodor Lynen Fellowship of the Alexander von Humboldt Foundation.
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Treusch, A., Vergin, K., Finlay, L. et al. Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3, 1148–1163 (2009). https://doi.org/10.1038/ismej.2009.60
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