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Bacterioplankton Community Variation Across River to Ocean Environmental Gradients

  • Microbiology of Aquatic Systems
  • Published:
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Abstract

Coastal zones encompass a complex spectrum of environmental gradients that each impact the composition of bacterioplankton communities. Few studies have attempted to address these gradients comprehensively. We generated a synoptic, 16S rRNA gene-based bacterioplankton community profile of a coastal zone by applying the fingerprinting technique denaturing gradient gel electrophoresis to water samples collected from the Columbia River, estuary, and plume, and along coastal transects covering 360 km of the Oregon and Washington coasts and extending to the deep ocean (>2,000 m). Communities were found to cluster into five distinct groups based on location in the system (ANOSIM, p < 0.003): estuary, plume, epipelagic, shelf bottom (depth < 150 m), and slope bottom (depth > 650 m). Across all environments, abiotic factors (salinity, temperature, depth) explained most of the community variability (ρ = 0.734). But within each coastal environment, biotic factors explained most of the variability. Thus, structuring physical factors in coastal zones, such as salinity and temperature, define the boundaries of many distinct microbial habitats, but within these habitats variability in microbial communities is explained by biological gradients in primary and secondary productivity.

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References

  1. Alonso-Saez L, Aristegui J, Pinhassi J, Gomez-Consarnau L, Gonzalez JM, Vaque D, Agusti S, Gasol JM (2007) Bacterial assemblage structure and carbon metabolism along a productivity gradient in the NE Atlantic Ocean. Aquat Microb Ecol 46:43–53

    Article  Google Scholar 

  2. Bernhard AE, Colbert D, McManus J, Field KG (2005) Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries. FEMS Microbiol Ecol 52:115–128

    Article  PubMed  CAS  Google Scholar 

  3. Bouvier TC, PAd G (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470

    Article  CAS  Google Scholar 

  4. Casamayor EO, Schafer H, Baneras L, Pedros-Alio C, Muyzer G (2000) Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol 66:499–508

    Article  PubMed  CAS  Google Scholar 

  5. Celussi M, Cataletto B, Umani SF, Del Negro P (2009) Depth profiles of bacterioplankton assemblages and their activities in the Ross Sea. Deep Sea Res Part I Oceanogr Res Pap 56:2193–2205

    Article  CAS  Google Scholar 

  6. Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219

    Article  Google Scholar 

  7. Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga–Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697

    Article  PubMed  CAS  Google Scholar 

  8. Crump BC, Baross JA, Simenstad CA (1998) Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquat Microb Ecol 14:7–18

    Article  Google Scholar 

  9. 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

    PubMed  CAS  Google Scholar 

  10. Crump BC, Baross JA (2000) Archaeaplankton in the Columbia River, its estuary and the adjacent coastal ocean, USA. FEMS Microbiol Ecol 31:231–239

    Article  PubMed  CAS  Google Scholar 

  11. Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69:2253–2268

    Article  PubMed  Google Scholar 

  12. 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Crump BC, Peranteau C, Beckingham B, Cornwell JC (2007) Respiratory succession and community succession of bacterioplankton in seasonally anoxic estuarine waters. Appl Environ Microbiol 73:6802–6810

    Article  PubMed  CAS  Google Scholar 

  15. Ferrari VC, Hollibaugh JT (1999) Distribution of microbial assemblages in the Central Arctic Ocean Basin studied by PCR/DGGE: analysis of a large data set. Hydrobiologia 401:55–68

    Article  CAS  Google Scholar 

  16. Fierer N, Carney KM, Horner-Devine MC, Megonigal JP (2009) The biogeography of ammonia-oxidizing bacterial communities in soil. Microb Ecol 58:435–445

    Article  PubMed  Google Scholar 

  17. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA 105:7774–7778

    Article  PubMed  CAS  Google Scholar 

  18. Ghiglione JF, Palacios C, Marty JC, Mevel G, Labrune C, Conan P, Pujo-Pay M, Garcia N, Goutx M (2008) Role of environmental factors for the vertical distribution (0–1000 m) of marine bacterial communities in the NW Mediterranean Sea. Biogeosci Discuss 5:1751–1764

    Article  CAS  Google Scholar 

  19. Gordon LI, Jennings JC, Ross AA, Krest JM (1994) A suggested protocol for continuous flow analysis of seawater nutrients (phosphate, nitrate, nitrite, and silicic acid) in the WOCE Hydrographic Program and the Joint Global Ocean Fluxes Study. WHP Office Report 91: Revision 1, Nov. 1994

  20. Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043

    Article  PubMed  CAS  Google Scholar 

  21. Hewson I, Fuhrman JA (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70:3425–3433

    Article  PubMed  CAS  Google Scholar 

  22. Hewson I, Capone DG, Steele JA, Fuhrman JA (2006) Influence of Amazon and Orinoco offshore surface water plumes on oligotrophic bacterioplankton diversity in the west tropical Atlantic. Aquat Microb Ecol 43:11–22

    Article  Google Scholar 

  23. Hewson I, Steele JA, Capone DG, Fuhrman JA (2006) Temporal and spatial scales of variation in bacterioplankton assemblages of oligotrophic surface waters. Mar Ecol Prog Ser 311:67–77

    Article  Google Scholar 

  24. Hickey BM (1989) Patterns and processes of shelf ecosystems and slope circulation. In: Landry MR, Hickey BM (eds) Coastal oceanography of Washington and Oregon. Elsevier, Amsterdam, pp 41–115

    Chapter  Google Scholar 

  25. Hickey BM, Pietrafesa LJ, Jay DA, Boicourt WC (1998) The Columbia River plume study: subtidal variability in the velocity and salinity fields. J Geophys Res Oceans 103:10339–10368

    Article  CAS  Google Scholar 

  26. Hickey BM, Banas NS (2003) Oceanography of the US Pacific Northwest Coastal Ocean and estuaries with application to coastal ecology. Estuaries 26:1010–1031

    Article  Google Scholar 

  27. Hickey BM, Banas NS (2008) Why is the northern end of the California Current System so productive? Oceanography 21:90–107

    Google Scholar 

  28. Hickey BM, Kudela RM, Nash JD, Bruland KW, Peterson WT, MacCready P, Lessard EJ, Jay DA, Banas NS, Baptista AM, Dever EP, Kosro PM, Kilcher LK, Horner-Devine AR, Zaron ED, McCabe RM, Peterson JO, Orton PM, Pan J, Lohan MC (2010) River influences on shelf ecosystems: introduction and synthesis. J Geophys Res-Oceans 115(C00B17):1–26

    Google Scholar 

  29. Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM (2004) A taxa–area relationship for bacteria. Nature 432:750–753

    Article  PubMed  CAS  Google Scholar 

  30. Janse I, Kardinaal WEA, Meima M, Fastner J, Visser PM, Zwart G (2004) Toxic and nontoxic microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Appl Environ Microbiol 70:3979–3987

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  32. Kataoka T, Hodoki Y, Suzuki K, Saito H, Higashi S (2009) Tempo-spatial patterns of bacterial community composition in the western North Pacific Ocean. J Mar Syst 77:197–207

    Article  Google Scholar 

  33. Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47

    Article  PubMed  CAS  Google Scholar 

  34. Kirchman DL, Keil RG, Simon M, Welschmeyer NA (1993) Biomass and production of heterotrophic bacterioplankton in the oceanic sub-arctic Pacific. Deep Sea Res Pt I Oceanogr Res Pap 40:967–988

    Article  Google Scholar 

  35. Kosro PM (2005) On the spatial structure of coastal circulation off Newport, Oregon, during spring and summer 2001 in a region of varying shelf width. J Geophys Res-Oceans 110(C10S06):1–16

    Google Scholar 

  36. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  PubMed  CAS  Google Scholar 

  37. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  38. Long RA, Azam F (2001) Microscale patchiness of bacterioplankton assemblage richness in seawater. Aquat Microb Ecol 26:103–113

    Article  Google Scholar 

  39. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci 104:11436–11440

    Article  PubMed  CAS  Google Scholar 

  40. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  PubMed  CAS  Google Scholar 

  41. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  Google Scholar 

  42. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P, Tunlid A, Hagstrom A (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16:867–880

    Article  PubMed  CAS  Google Scholar 

  43. Riemann L, Steward GF, Fandino LB, Campbell L, Landry MR, Azam F (1999) Bacterial community composition during two consecutive NE Monsoon periods in the Arabian Sea studied by denaturing gradient gel electrophoresis (DGGE) of rRNA genes. Deep Sea Res Part II Top Stud Oceanogr 46:1791–1811

    Article  Google Scholar 

  44. 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

    Article  Google Scholar 

  45. Simek K, Pernthaler J, Weinbauer MG, Hornak K, Dolan JR, Nedoma J, Masin M, Amann R (2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl Environ Microbiol 67:2723–2733

    Article  PubMed  CAS  Google Scholar 

  46. Sugimura Y, Suzuki Y (1988) A high-temperature catalytic oxidation method for the determination of non-volatile dissolved organic carbon in seawater by direct injection of a liquid sample. Mar Chem 24:105–131

    Article  CAS  Google Scholar 

  47. Troussellier M, Schafer 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

    Article  Google Scholar 

  48. Valderrama JC (1981) The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Mar Chem 10:109–122

    Article  CAS  Google Scholar 

  49. Vieira RP, Gonzalez AM, Cardoso AM, Oliveira DN, Albano RM, Clementino MM, Martins OB, Paranhos R (2008) Relationships between bacterial diversity and environmental variables in a tropical marine environment, Rio de Janeiro. Environ Microbiol 10:189–199

    PubMed  CAS  Google Scholar 

  50. Wright SW, Jeffrey SW, Mantoura RFC, Llewellyn CA, Bjornland T, Repeta D, Welschmeyer N (1991) Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar Ecol Prog Ser 77:183–196

    Article  CAS  Google Scholar 

  51. Zhou JZ, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    PubMed  CAS  Google Scholar 

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Acknowledgments

This study was carried out within the context of the Science and Technology Center for Coastal Marine Observation & Prediction (CMOP) supported by the National Science Foundation (grant number OCE-0424602 to Antonio Baptista). We thank the crew of the R/V Wecoma, Lydie Herfort for field planning and assistance, Joanna Green and Erica Kiss for bacterial production measurements and laboratory assistance, Suzanne DeLorenzo-Kroll and Daniel Murphy for help in sample collection, and Joe Jennings, Marnie Jo Zirbel, and Ricardo Letelier for inorganic nutrient and pigment analyses.

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  1. Horn Point Laboratory, University of Maryland Center for Environmental Science, Cambridge, MD, USA

    Caroline S. Fortunato & Byron C. Crump

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  1. Caroline S. Fortunato
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  2. Byron C. Crump
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Correspondence to Caroline S. Fortunato.

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Fortunato, C.S., Crump, B.C. Bacterioplankton Community Variation Across River to Ocean Environmental Gradients. Microb Ecol 62, 374–382 (2011). https://doi.org/10.1007/s00248-011-9805-z

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