Biodiversity Science ›› 2011, Vol. 19 ›› Issue (6): 770-778.doi: 10.3724/SP.J.1003.2011.09149

Special Issue: Marine Biodiversity Studies in China Seas

• Special Issue • Previous Article     Next Article

Bacterial community biodiversity in estuaries and its controlling factors: a case study in Chesapeake Bay

Jinjun Kan1*, Jun Sun2   

  1. 1 Stroud Water Research Center, 970 Spencer Road, Avondale, PA 19311, USA

    2 College of Marine Science and Engineering, Tianjin University of Science and Technology, Tianjin 300457, China
  • Received:2011-08-24 Revised:2011-11-30 Online:2011-12-19
  • Jinjun Kan E-mail:jkan@stroudcenter.org
  • Supported by:

    Christina River Basin Critical Zone Observatory (CZO): Spatial and temporal integration of carbon and mineral fluxes: a whole watershed approach to quantifying anthropogenic modification of critical zone carbon sequestration (NSF 2010-2015)

Estuaries are among the most productive and dynamic aquatic ecosystems on earth, due to the mixing of fresh and salt waters and significant recycling of nutrients and organic matters. Sitting in a transitional zone, bacterial communities in an estuary typically harbor representatives of both freshwater and marine groups: Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Cyanobacteria (Synechococcus), Bacteroidetes, Actinobacteria, and Verrucomicrobia. In addition, estuaries such as Chesapeake Bay also contain their own unique bacterial signatures including the SAR11 group, Roseobacter, SAR86, and Actinobacteria subclades, suggesting the ecological adaptation of organisms endemic to the Bay or perhaps, to large temperate estuaries in general. Relative to spatial variations, remarkable seasonal shifts and recurring annual patterns were identified in Chesapeake Bay bacterial communities. Besides water residence time and bacterial growth rate, many other factors are potential driving forces for the microbial diversity and bacterial population dynamics we observed. Temporal variations in bacterial communities were best explained by change in chlorophyll a (Chl a) and water temperature, while other factors such as dissolved oxygen, ammonia, nitrite and nitrate, and viral abundance also appeared to contribute to seasonal succession. Recently, the applications applications of community-based genomics and postgenomics (transcriptomics and proteomics) have allowed us to study the comprehensive gene diversity and gene expression directly from natural microbial communities. We predict that further studies and analyses of these genes and proteins will deliver new discoveries regarding the composition and function of microbial communities in aquatic environments.

Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol, 172: 762-770.

Béjà O, Spudich EN, Spudich JL, Leclerc M, DeLong EF (2001) Proteorhodopsin phototrophy in the ocean. Nature, 411:786-789.

Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich SB, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF (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, Villacorta R, Amjadi M, Garrigues C, Jovanovich SB, Feldman RA, DeLong EF (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, Sayers EW (2011) GenBank. Nucleic Acids Res, 39: D32–D37.

Bouvier TC, del Giorgio P A (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr, 47: 453-470.

Button DK, Schut F, Quang P, Martin R, Robertson BR (1993) Viability and isolation of marine bacteria by dilution culture: theory, procedures, and initial results. Appl Environ Microbiol, 59:881-891.

Cho JC, Giovannoni SJ (2004b) Cultivation and growth characteristics of a diverse group of oligotrophic marine ?-Proteobacteria. Appl Environ Microbiol, 70:432-440.

Cho JC, Vergin KL, Morris RM, Giovannoni SJ (2004a) Lentisphaera araneosa gen. Nov., sp. nov., a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum, Lentisphaerae. Environ Microbiol, 6:611-621.

Conway T, Schoolnik GK (2003) Microarray expression profiling: capturing a genome-wide protrait of the transcriptome. Mol Microbiol, 47:879-889.

Cottrell MT, Waidner LA, Yu L, Kirchman DL (2005) Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environ Microbiol, 7:1883-1895.

Crump BC, Hobbie JE (2005) Synchrony and seasonality in bacterioplankton diversity of two temperate rivers. Limnol Oceanogr, 50:1718-1729.

Crump BC, Peterson BJ, Raymond PA, Amon RMW, Rinehart A, McClelland JW, Holmes RM (2009) Circumpolar Synchrony in Big River Bacterioplankton. Proc Natl Acad Sci USA, 106: 21208–21212.

Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol, 70:1494-1505.

Crump BC, Armbrust EV, Baross JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl Environ Microbiol, 65: 3192-3204.

Daley RJ, Hobbie JE (1975) Direct counts of aquatic bacteria by a modified epifluorescent technique. Limnol Oceanogr, 20:875-882.

de la Torre JR, Christianson LM, Béjà O, Suzuki MT, Karl DM, Heidelberg J, DeLong EF (2003) Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc Natl Acad Sci USA, 100:12830-12835.

del Giorgio PA, Bouvier TC (2002) Linking the physiological and phylogenetic succession in free-living bacterial communities along an estuarine salinity gradient. Limnol Oceanogr, 47:471-486.

DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U, Martinez A, Sullivan MB, Edwards R, Brito BR, Chisholm SW, Karl DM (2006) Community genomics among stratified microbial assemblages in the ocean's interior. Science, 311:496-503.

Eymann C, Homuth G, Scharf C, Hecker M (2002) Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol, 184:2500-2520.

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.

Giovannoni SJ, Rappé MS (2000) Evolution, diversity, and molecular ecology of marine prokaryotes. In: Microbial ecology of the oceans (ed Kirchman DL), pp. 47-84.Wiley-Liss, New York

Giovannoni SJ, Britschgi TB, Moyer CL, Field KG (1990) Genetic diversity in Sargasso Sea bacterioplankton. Nature, 345: 60-63.

Glibert PM, Conley DJ, Fisher TR, Harding LWJ, Malone TC (1995) Dynamics of the 1990 Winter/Spring bloom in Chesapeake Bay. Mar Ecol Prog Ser, 122:27-43.

Heidelberg JF, Heidelberg KB, Colwell RR (2002) Seasonality of Chesapeake Bay bacterioplankton species. Appl Environ Microbiol, 68: 5488-5497.

Henriques IS, Alves A, Tacao M, Almeida A, Cunha A, Correia A (2006) Seasonal and spatial variability of free-living bacterial community composition along an estuarine gradient (Ria de Aveiro, Portugal). Estuar Coast Shelf S, 68:139-148.

Henriques IS, Almeida MA, Cunha MA, Correia A (2004) Molecular sequence analysis of prokaryotic diversity in the middle and outer sections of the Portuguese estuary Ria de Aveiro. FEMS Microbiol Ecol, 49:269-279.

Hewson I, Fuhrman J A (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol, 70:3425-33.

Hollibaugh JT, Wong PS, Murrell MC (2000) Similarity of particle-associated and free-living bacterial communities in northern San Francisco Bay, California. Aquat Microb Ecol, 21:103-109.

Hoppe HG (1976) Determination and properties of actively metabolizing heterotrophic bacteria in the sea, investigated by the means of micro-autoradiography. Mar Biol, 36:291-302.

Jannasch HW, Jones GE (1959) Bacterial populations in sea water as determined by different methods of enumeration. Limnol Oceanogr, 4:128-139.

Jonas RB, Tuttle JH (1990) Bacterioplankton and organic carbon dynamics in the lower mesohaline Chesapeake Bay. Appl Environ Microbiol, 56:747-757.

Kan J, Chen F (2004) Co-monitoring bacterial and dinoflagellates communities by denaturing gradient gel electrophoresis (DGGE) and SSU rDNA sequencing during a dinoflagellate bloom. Acta Oceanol Sin, 23: 483-492.

Kan J, Crump BC, Wang K, Chen F (2006b) Bacterioplankton community in Chesapeake Bay: Predictable or random assemblages. Limnol Oceanogr, 51:2157-2169.

Kan J, Wang K, Chen F (2006a) Temporal variation and detection limit of an estuarine bacterioplankton community analyzed by denaturing gradient gel electrophoresis (DGGE). Aquat Microb Ecol, 42:7-18.

Kan J, Suzuki M, Wang K, Evans SE, Chen F (2007) High temporal but low spatial heterogeneity of bacterioplankton in the Chesapeake Bay. Appl Environ Microbiol, 73:6776-6789.

Kan J, Evans SE, Chen F, Suzuki MT (2008) Novel estuarine bacterioplankton in rRNA operon libraries from the Chesapeake Bay. Aquat Microb Ecol, 51:55-66.

Kan J, Hanson TE, Ginter JM, Wang K, Chen F (2005) Metaproteomic analysis of Chesapeake Bay microbial communities. Saline Systems, 1:7.

Kan J, Hanson TE, Chen F (2011) Synchronicity between population structure and proteome profiles: a metaproteomic analysis of Chesapeake Bay bacterial communities. In: Handbook of Molecular Microbial Ecology, Volume I: Metagenomics and Complementary Approaches (ed de Bruijn FJ) pp. 637-644.Wiley-Blackwell, Hoboken.

Kent AD, Jones SE, Yannarell AC, Graham JM, Lauster GH, Kratz TK, Triplett EW (2004) Annual patterns in bacterioplankton community variability in a humic lake. Microb Ecol, 48: 550-560.

Kirchman DL, Rich JH (1997) Regulation of bacterial growth rates by dissolved organic carbon and temperature in the equatorial Pacific Ocean. Microb Ecol, 33:11-20.

Lopez MF (1999) Proteome analysis I. Gene products are where the biological action is. J Chromatogr, 722:191-202.

Malone TC, Kemp WM, Ducklow HW, Boynton WR, Tuttle JH, Jonas RB (1986) Lateral variation in the production and fate of phytoplankton in a partially stratified estuary. Mar Ecol Prog Ser, 32:149-160.

Monsen NE, Cloern JE, Lucas LV, Monismith SG (2002) A comment on the use of flushing time, residence time, and age as transport time scales. Limnol Oceanogr, 47:1545-1553.

Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K, DeLong EF (1998) Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol, 64:2585-2595.

Nixon SW, Ammerman JW, Atkinson LP, Berounsky VM, Billen G, Boicourt WC, Boynton WR, Church TM, Ditoro DM, Elmgren R, Garber JH, Giblin AE, Jahnke RA, Owens NJP, Pilson MEQ, Seitzinger SP (1996) The fate of nitrogen and phosphorus at the land sea margin of the North Atlantic Ocean. Biogeochemistry, 35:141-180.

Olsen GJ, Lane DJ, Giovannoni J, Pace NR (1986) Microbial ecology and evolution: a ribosomal RNA approach. Ann Rev Microbiol, 40:337-365.

Pace NR, Stahl DA, Olsen GJ, Lane DJ (1985) Analyzing natural microbial populations by rRNA sequences. Amer Soc Microbiol News, 51:4-12.

Pernthaler J, Gl?ckner FO, Unterholzner S, Alfreider A, Psenner R, Amann R (1998) Seasonal community and population dynamics of pelagic bacteria and archaea in a high mountain lake. Appl Environ Microbiol, 64:4299-4306.

Petersohn A, Brigulla M, Haas S, Hoheisel JD, Volker U, Hecker M (2001) Global analysis of the general stress response of Bacillus subtilis. J Bacteriol, 183:5617-5631.

Pinhassi M, Sala M, Havskum H, Peters F, Guadayol O, Malits A, Marrase C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol, 70:6753-6766.

Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol, 23:187-204.

Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr, 25:943-948.

Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake II RC, Shah M, Hettich RL, Banfield JF (2005) Community proteomics of a natural microbial biofilm. Science, 308:1915-1920.

Rappé MS, Cannon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature, 418:630-633.

Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol, 66: 578-587.

Riesenfeld CS, Schloss PD, Handelsman J (2004) Metagenomics: genomic analysis of microbial communities. Annu Rev Genet, 38:525-552.

Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, MacNeil IA, Minor C, Tiong CL, Gulman M, Osburne MS, Clardy J, Handelsman J, Goodman RM (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol, 66:2541-2547.

SAS Institute Inc (1992) SAS user's guide. SAS Institute Inc.

Sekiguchi H, Watanabe M, Nakahara T, Xu B, Uchiyama H (2002) Succession of bacterial community structure along the Changjiang River determined by denaturing gradient gel electrophoresis and clone library analysis. Appl Environ Microbiol, 68:5142-5150.

Selje N, Simon M (2003) Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. Aquat Microb Ecol, 30:221-237.

Shiah F-K, Ducklow HW (1994) Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate. Limnol Oceanogr, 39:1243-1258.

Smith EM, Kemp WM (2003) Planktonic and bacterial respiration along an estuarine gradient: response to carbon and nutrient enrichment. Aquat Microb Ecol, 30:251-261.

Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol, 39:321-346.

Sun J, Feng YY, Zhang YH, Hutchins DA (2007) Fast microzooplankton grazing on fast-growing, low-biomass phytoplankton - A case study in spring in the Chesapeake Bay, Delaware Inland Bays and the Delaware Bay. Hydrobiology, 589(1): 127-139.

Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, Podar M, Short JM, Mathur EJ, Detter JC, Bork P, Hugenholtz P, Rubin EM (2005) Comparative metagenomics of microbial communities. Science, 308:554-557.

Troussellier M, Sch?fer H, Batailler N, Bernard L, Courties C, Lebaron P, Muyzer G, Servais P, Vives-Rego J (2002) Bacterial activity and genetic richness along an estuarine gradient (Rhone River plume, France). Aquat Microb Ecol, 28:13-24.

Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (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, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304:66-74.

Wasinger VC, Cordwell SJ, Cerpa Poljak A, Yan JX, Gooley AA, Wilkins MR, Duncan MW, Harris R, Williams KL, Humphery-Smith I (1995) Progress with gene product mapping of Moli cutes: Mycoplasma genitalium. Electrophoresis, 16:1090-1094.

Wikner J, Hagstr?m A (1991) Annual study of bacterioplankton community dynamics. Limnol Oceanogr, 36:1313-1324.

Wilmes P, Bond PL (2004) The application of two-dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms. Environ Microbiol, 6:911-920.

ZoBell CE (1946) Marine Microbiology. Chronica botanica, Waltham, Mass.
No related articles found!
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed