Estuaries and Coasts

, Volume 36, Issue 5, pp 1073–1083 | Cite as

Dark Carbon Fixation in the Columbia River’s Estuarine Turbidity Maxima: Molecular Characterization of Red-Type cbbL Genes and Measurement of DIC Uptake Rates in Response to Added Electron Donors

  • S. L. Bräuer
  • K. Kranzler
  • N. Goodson
  • D. Murphy
  • H. M. Simon
  • A. M. Baptista
  • B. M. Tebo


Dark CO2 fixation has been shown to rival the importance of oxygenic photosynthesis in the global carbon cycle, especially in stratified environments, such as salt wedge estuaries. We investigated this process in the Columbia River estuary using a variety of techniques including functional gene cloning of cbbL (the large subunit of form I RuBisCO), quantitative real-time PCR (qPCR) estimations of cbbL abundance, and analyses of stimulated 14C-bicarbonate assimilation. A diversity of red-type cbbL genes were retrieved from clone libraries, with 28 unique operational taxonomic units determined from 60 sequences. The majority of the sequences formed two clusters that were distinct from the major clusters typically found in soil environments, revealing the presence of a unique community of autotrophic or facultatively autotrophic/mixotrophic microorganisms in the Columbia River estuary. qPCR estimates indicated that roughly 0.03–0.15 % of the microbial population harbored the cbbL gene, with greater numbers of total bacteria and cbbL gene copies found in the estuarine turbidity maxima (ETM) compared to non-ETM events. In vitro incubations with radiolabeled bicarbonate indicated maximum stimulation by thiosulfate and also suggested that a diversity of other potential electron donors may stimulate CO2 fixation, including nitrite, ammonium, and Mn(II). Taken together, these results highlight the diversity of the microbial metabolic strategies employed and emphasize the importance of dark CO2 fixation in the dynamic waters of the Columbia River estuary despite the abundance of organic material.


Estuary Bacteria Carbon fixation Autotrophy Mn oxidation RuBisCO cbbL qPCR 

Supplementary material

12237_2013_9603_MOESM1_ESM.pdf (292 kb)
ESM 1(PDF 291 kb)


  1. Aguilar-Islas, A.M., and K.W. Bruland. 2006. Dissolved manganese and silicic acid in the Columbia River plume: a major source to the California current and coastal waters off Washington and Oregon. Marine Chemistry 101: 233–247.CrossRefGoogle Scholar
  2. Alfreider, A., C. Vogt, M. Geiger-Kaiser, and R. Psenner. 2009. Distribution and diversity of autotrophic bacteria in groundwater systems based on the analysis of RubisCO genotypes. Systematic and Applied Microbiology 32: 140–150.CrossRefGoogle Scholar
  3. Alonso-Saez, L., P.E. Galand, E.O. Casamayor, C. Pedros-Alio, and S. Bertilsson. 2010. High bicarbonate assimilation in the dark by Arctic bacteria. ISME Journal 4: 1581–1590.CrossRefGoogle Scholar
  4. Badger, M.R., and E.J. Bek. 2008. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. Journal of Experimental Botany 59: 1525–1541.CrossRefGoogle Scholar
  5. Baptista, A.M., Y.L. Zhang, A. Chawla, M. Zulauf, C. Seaton, E.P. Myers, J. Kindle, M. Wilkin, M. Burla, and P.J. Turner. 2005. A cross-scale model for 3D baroclinic circulation in estuary–plume–shelf systems: II. Application to the Columbia River. Continental Shelf Research 25: 935–972.CrossRefGoogle Scholar
  6. Barnes, C., A. Duxbury, and B. Morse. 1972. Circulation and selected properties of the Columbia River effluent at sea. In The Columbia River estuary and adjacent ocean waters, ed. A. Pruter and D. Alverson, 41–80. Seattle, WA: University of Washington Press.Google Scholar
  7. Baross, J., B. Crump, and C.A. Simenstad. 1994. Elevated 'microbial loop' activities in the Columbia River estuary turbidity maximum. In Changing particle fluxes in estuaries: implications from science to management. ESCAERF22 Symposium, ed. K. Dyer and R. Orth, 459–464. Fiedensborg, Denmark: Olsen & Olsen.Google Scholar
  8. Berhane, I., R.W. Sternberg, G.C. Kineke, T.G. Milligan, and K. Kranck. 1997. The variability of suspended aggregates on the Amazon Continental Shelf. Continental Shelf Research 17: 267–285.CrossRefGoogle Scholar
  9. Biggs, R.B., J.H. Sharp, T.M. Church, and J.M. Tramontano. 1983. Optical-properties, suspended sediments, and chemistry associated with the turbidity maxima of the Delaware Estuary. Canadian Journal of Fisheries and Aquatic Sciences 40: 172–179.CrossRefGoogle Scholar
  10. Bräuer, S.L., C. Adams, K. Kranzler, D. Murphy, M. Xu, P. Zuber, H.M. Simon, A.M. Baptista, and B.M. Tebo. 2011. Culturable Rhodobacter and Shewanella species are abundant in estuarine turbidity maxima of the Columbia River. Environmental Microbiology 13: 589–603.CrossRefGoogle Scholar
  11. Breuker, A., G. Koeweker, A. Blazejak, and A. Schippers. 2011. The deep biosphere in terrestrial sediments in the Chesapeake Bay area, Virginia, USA. Frontiers in Microbiology 2: 156. doi:10.3389/fmicb.2011.00156.CrossRefGoogle Scholar
  12. Bruland, K.W., M.C. Lohan, A.M. Aguilar-Islas, G.J. Smith, B. Sohst, and A. Baptista. 2008. Factors influencing the chemistry of the near-field Columbia River plume: nitrate, silicic acid, dissolved Fe, and dissolved Mn. Journal of Geophysical Research Oceans 113: C00B02. doi:10.1029/2007JC004702.CrossRefGoogle Scholar
  13. Burla M. 2009. The Columbia River estuary and plume: natural variability, anthropogenic change and physical habitat for salmon. PhD thesis, Oregon Health & Science University, Beaverton, ORGoogle Scholar
  14. Casamayor, E.O., J. Garcia-Cantizano, and C. Pedros-Alio. 2008. Carbon dioxide fixation in the dark by photosynthetic bacteria in sulfide-rich stratified lakes with oxic–anoxic interfaces. Limnology and Oceanography 53: 1193–1203.CrossRefGoogle Scholar
  15. Casamayor, E.O., J. Garcia-Cantizano, J. Mas, and C. Pedros-Alio. 2001. Primary production in estuarine oxic/anoxic interfaces: contribution of microbial dark CO2 fixation in the Ebro River salt wedge estuary. Marine Ecology Progress Series 215: 49–56.CrossRefGoogle Scholar
  16. Casamayor, E.O., M. Lliros, A. Picazo, A. Barberan, C.M. Borrego, and A. Camacho. 2012. Contribution of deep dark fixation processes to overall CO2 incorporation and large vertical changes of microbial populations in stratified karstic lakes. Aquatic Sciences 74: 61–75.CrossRefGoogle Scholar
  17. Caspi, R., M.G. Haygood, and B.M. Tebo. 1996. Unusual ribulose-1,5-bisphosphate carboxylase/oxygenase genes from a marine manganese-oxidizing bacterium. Microbiology 142: 2549–2559.CrossRefGoogle Scholar
  18. Cochran, P.K., and J.H. Paul. 1998. Seasonal abundance of lysogenic bacteria in a subtropical estuary. Applied and Environmental Microbiology 64: 2308–2312.Google Scholar
  19. Colbert, D., and J. McManus. 2003. Nutrient biogeochemistry in an upwelling-influenced estuary of the Pacific Northwest (Tillamook Bay, Oregon, USA). Estuaries and Coasts 26: 1205–1219.CrossRefGoogle Scholar
  20. Cottrell, M.T., J. Ras, and D.L. Kirchman. 2010. Bacteriochlorophyll and community structure of aerobic anoxygenic phototrophic bacteria in a particle-rich estuary. The ISME Journal 4: 945–954.CrossRefGoogle Scholar
  21. Crump, B.C., and J.A. Baross. 1996. Particle-attached bacteria and heterotrophic plankton associated with the Columbia River estuarine turbidity maxima. Marine Ecology Progress Series 138: 265–273.CrossRefGoogle Scholar
  22. Crump, B.C., and J.A. Baross. 2000. Characterization of the bacterially-active particle fraction in the Columbia River estuary. Marine Ecology Progress Series 206: 13–22.CrossRefGoogle Scholar
  23. Crump, B.C., J.A. Baross, and C.A. Simenstad. 1998. Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquatic Microbial Ecology 14: 7–18.CrossRefGoogle Scholar
  24. Crump, B.C., E.V. Armbrust, and J.A. Baross. 1999. Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Applied and Environmental Microbiology 65: 3192–3204.Google Scholar
  25. DeLorenzo, S., S.L. Bräuer, C.A. Edgmont, L. Herfort, B.M. Tebo, and P. Zuber. 2012. Ubiquitous dissolved inorganic carbon assimilation by marine bacteria in the Pacific Northwest coastal ocean as determined by stable isotope probing. PLoS One 7: e46695.CrossRefGoogle Scholar
  26. Demaster, D.J., S.A. Kuehl, and C.A. Nittrouer. 1986. Effects of suspended sediments on geochemical processes near the mouth of the Amazon River—examination of biological silica uptake and the fate of particle-reactive elements. Continental Shelf Research 6: 107–125.CrossRefGoogle Scholar
  27. Dick, G.J., S. Podell, H.A. Johnson, Y. Rivera-Espinoza, R. Bernier-Latmani, J.K. McCarthy, J.W. Torpey, B.G. Clement, T. Gaasterland, and B.M. Tebo. 2008. Genomic insights into Mn(II) oxidation by the marine alphaproteobacterium Aurantimonas sp. strain SI85-9A1. Applied and Environmental Microbiology 74: 2646–2658.CrossRefGoogle Scholar
  28. Doronia, N.V., and Y.A. Trotsenko. 1985. Levels of carbon dioxide assimilation in bacteria with different pathways of C1 metabolism. Mikrobiologiya 53: 885–889.Google Scholar
  29. Elsaied, H., and T. Naganuma. 2001. Phylogenetic diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from deep-sea microorganisms. Applied and Environmental Microbiology 67: 1751–1765.CrossRefGoogle Scholar
  30. Etcheber, H., A. Taillez, G. Abril, J. Garnier, P. Servais, F. Moatar, and M.V. Commarieu. 2007. Particulate organic carbon in the estuarine turbidity maxima of the Gironde, Loire and Seine estuaries: origin and lability. Hydrobiologia 588: 245–259.CrossRefGoogle Scholar
  31. Felsenstein J. 2004. PHYLIP (Phylogeny Inference Package) version 3.68. Department of Genome Sciences, University of Washington, Seattle (distributed by the author).Google Scholar
  32. Fey, A., S. Eichler, S. Flavier, R. Christen, M.G. Hofle, and C.A. Guzman. 2004. Establishment of a real-time PCR-based approach for accurate quantification of bacterial RNA targets in water, using Salmonella as a model organism. Applied and Environmental Microbiology 70: 3618–3623.CrossRefGoogle Scholar
  33. Fortunato, C.S., L. Herfort, P. Zuber, A.M. Baptista, and B.C. Crump. 2012. Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient. The ISME Journal 6: 554–563.CrossRefGoogle Scholar
  34. Frolov, S., A.M. Baptista, Y.L. Zhang, and C. Seaton. 2009. Estimation of ecologically significant circulation features of the Columbia River estuary and plume using a reduced-dimension Kalman filter. Continental Shelf Research 29: 456–466.CrossRefGoogle Scholar
  35. Garcia-Cantizano, J., E.O. Casamayor, J.M. Gasol, R. Guerrero, and C. Pedros-Alio. 2005. Partitioning of CO2 incorporation among planktonic microbial guilds and estimation of in situ specific growth rates. Microbial Ecology 50: 230–241.CrossRefGoogle Scholar
  36. Garel, E., L. Pinto, A. Santos, and O. Ferreira. 2009. Tidal and river discharge forcing upon water and sediment circulation at a rock-bound estuary (Guadiana estuary, Portugal). Estuarine, Coastal and Shelf Science 84: 269–281.CrossRefGoogle Scholar
  37. Gelfenbaum, G. 1983. Suspended sediment response to semidiurnal and fortnightly tidal variations in a mesotidal estuary—Columbia River, USA. Marine Geology 52: 39–57.CrossRefGoogle Scholar
  38. Gilbert, M., Needoba, J.N., Koch, C., Barnard, A., and Baptista A.M. (2013). Nutrient loading and transformations in the Columbia River estuary determined by high resolution in situ sensors. Estuaries and Coasts. doi:10.1007/s12237-013-9597-0.
  39. Glaubitz, S., M. Labrenz, G. Jost, and K. Jürgens. 2010. Diversity of active chemolithoautotrophic prokaryotes in the sulfidic zone of a Black Sea pelagic redoxcline as determined by rRNA-based stable isotope probing. FEMS Microbiology Ecology 74: 32–41.CrossRefGoogle Scholar
  40. Glaubitz, S., T. Lueders, W.-R. Abraham, G. Jost, K. Jürgens, and M. Labrenz. 2009. 13C-isotope analyses reveal that chemolithoautotrophic gamma- and epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the Central Baltic Sea. Environmental Microbiology 11: 326–337.CrossRefGoogle Scholar
  41. González, J.M., B. Fernández-Gómez, A. Fernàndez-Guerra, et al. 2008. Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proceedings of the National Academy of Sciences 105: 8724–8729.CrossRefGoogle Scholar
  42. Good, I.J. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40: 237–264.Google Scholar
  43. Grabemann, I., R.J. Uncles, G. Krause, and J.A. Stephens. 1997. Behaviour of turbidity maxima in the Tamar (UK) and Weser (FRG) estuaries. Estuarine, Coastal and Shelf Science 45: 235–246.CrossRefGoogle Scholar
  44. Hall T. 2001. BioEdit version 5.0.6. . North Carolina State University, Department of Microbiology.
  45. Henry, S., D. Bru, B. Stres, S. Hallet, and L. Philippot. 2006. Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Applied and Environmental Microbiology 72: 5181–5189.CrossRefGoogle Scholar
  46. Henry, S., E. Baudoin, J.C. López-Gutiérrez, F. Martin-Laurent, A. Brauman, and L. Philippot. 2004. Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. Journal of Microbiological Methods 59: 327–335.CrossRefGoogle Scholar
  47. Herfort, L., T. Peterson, L. McCue, and P. Zuber. 2011. Protist 18S rRNA gene sequence analysis reveals multiple sources of organic matter contributing to turbidity maxima of the Columbia River estuary. Marine Ecology Progress Series 438: 19–31.CrossRefGoogle Scholar
  48. Herfort, L., T. Peterson, F. Prahl, L. McCue, J. Needoba, B. Crump, G. Roegner, V. Campbell, and P. Zuber. 2012. Red waters of Myrionecta rubra are biogeochemical hotspots for the Columbia River estuary with impacts on primary/secondary productions and nutrient cycles. Estuaries and Coasts 35: 878–891.CrossRefGoogle Scholar
  49. Horner-Devine, M.C., J.M. Silver, M.A. Leibold, et al. 2007. A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88: 1345–1353.CrossRefGoogle Scholar
  50. Huber, J.A., D.B. Mark Welch, H.G. Morrison, S.M. Huse, P.R. Neal, D.A. Butterfield, and M.L. Sogin. 2007. Microbial population structures in the deep marine biosphere. Science 318: 97–100.CrossRefGoogle Scholar
  51. Hügler, M., and S.M. Sievert. 2011. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annual Review of Marine Science 3: 261–289.CrossRefGoogle Scholar
  52. Indrebø, G., B. Pengerud, and I. Dundas. 1979. Microbial activities in a permanently stratified estuary. II. Microbial activities at the oxic–anoxic interface. Marine Biology 51: 305–309.CrossRefGoogle Scholar
  53. Islam, M.S., H. Ueda, and M. Tanaka. 2006. Spatial and seasonal variations in copepod communities related to turbidity maximum along the Chikugo estuarine gradient in the Upper Ariake Bay, Japan. Estuarine, Coastal and Shelf Science 68: 113–126.CrossRefGoogle Scholar
  54. Jassby, A.D., and T.M. Powell. 1994. Hydrodynamic influences on interannual chlorophyll variability in an estuary—Upper San-Francisco Bay Delta (California, USA). Estuarine, Coastal and Shelf Science 39: 595–618.CrossRefGoogle Scholar
  55. Jay, D.A., and J.D. Smith. 1990. Circulation, density distribution and neap-spring transitions in the Columbia River estuary. Progress in Oceanography 25: 81–112.CrossRefGoogle Scholar
  56. Jay, D.A., and J.D. Musiak. 1994. Particle trapping in estuarine tidal flows. Journal of Geophysical Research 99: 20445–20461.CrossRefGoogle Scholar
  57. Jones, S.E., and J.T. Lennon. 2010. Dormancy contributes to the maintenance of microbial diversity. Proceedings of the National Academy of Sciences 107: 5881–5886.CrossRefGoogle Scholar
  58. Jorgensen, B.B., J.G. Kuenen, and Y. Cohen. 1979. Microbial transformations of sulfur compounds in a stratified lake (Solar Lake, Sinai). Limnology and Oceanography 24: 799–822.CrossRefGoogle Scholar
  59. Jørgensen, B.B., H. Fossing, C.O. Wirsen, and H.W. Jannasch. 1991. Sulfide oxidation in the anoxic Black Sea chemocline. Deep Sea Research Part A. Oceanographic Research Papers 38(Supplement 2): S1083–S1103.CrossRefGoogle Scholar
  60. Jost, G., M. Zubkov, E. Yakushev, M. Labrenz, and K. Jurgens. 2008. High abundance and dark CO2 fixation of chemolithoautotrophic prokaryotes in anoxic waters of the Baltic Sea. Limnology and Oceanography 53: 14–22.CrossRefGoogle Scholar
  61. Kappenberg, J., and I. Grabemann. 2001. Variability of the mixing zones and estuarine turbidity maxima in the Elbe and Weser estuaries. Estuaries 24: 699–706.CrossRefGoogle Scholar
  62. Karl, D.M., and G.A. Knauer. 1991. Microbial production and particle flux in the upper 350 m of the Black Sea. Deep Sea Research Part A. Oceanographic Research Papers 38(Supplement 2): S921–S942.CrossRefGoogle Scholar
  63. Kellermann, C., D. Selesi, N. Lee, M. Hügler, J. Esperschütz, A. Hartmann, and C. Griebler. 2012. Microbial CO2 fixation potential in a tar-oil-contaminated porous aquifer. FEMS Microbiology Ecology 81: 172–187.CrossRefGoogle Scholar
  64. Kelly D. P. and A. P. Wood. 2006. The chemolithotrophic prokaryotes. In The prokaryotes: ecophysiology and biochemistry, vol. 2, edited by Dworkin M., E. Rosenberg and K.-H. Schleifer, 441–456. New York: Springer.Google Scholar
  65. Klinkhammer, G.P., and J. McManus. 2001. Dissolved manganese in the Columbia River estuary: production in the water column. Geochimica Et Cosmochimica Acta 65: 2835–2841.CrossRefGoogle Scholar
  66. Klinkhammer, G.P., C.S. Chin, C. Wilson, M.D. Rudnicki, and C.R. German. 1997. Distributions of dissolved manganese and fluorescent dissolved organic matter in the Columbia River estuary and plume as determined by in situ measurement. Marine Chemistry 56: 1–14.CrossRefGoogle Scholar
  67. Labrenz, M., G. Jost, C. Pohl, S. Beckmann, W. Martens-Habbena, and K. Jurgens. 2005. Impact of different in vitro electron donor/acceptor conditions on potential chemolithoautotrophic communities from marine pelagic redoxclines. Applied and Environmental Microbiology 71: 6664–6672.CrossRefGoogle Scholar
  68. Lennon, J.T., and S.E. Jones. 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Reviews Microbiology 9: 119–130.CrossRefGoogle Scholar
  69. Li, J.F., and C. Zhang. 1998. Sediment resuspension and implications for turbidity maximum in the Changjiang Estuary. Marine Geology 148: 117–124.CrossRefGoogle Scholar
  70. Lliros, M., L. Alonso-Saez, F. Gich, A. Plasencia, O. Auguet, E.O. Casamayor, and C.M. Borrego. 2011. Active bacteria and archaea cells fixing bicarbonate in the dark along the water column of a stratified eutrophic lagoon. FEMS Microbiology Ecology 77: 370–384.CrossRefGoogle Scholar
  71. Moran, M.A., A. Buchan, J.M. Gonzalez, et al. 2004. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432: 910–913.CrossRefGoogle Scholar
  72. Neretin, L.N., C. Pohl, G. Jost, T. Leipe, and F. Pollehne. 2003. Manganese cycling in the Gotland Deep, Baltic Sea. Marine Chemistry 82: 125–143.CrossRefGoogle Scholar
  73. Nielsen, E.S. 1952. The use of radioactive carbon (C14) for measuring organic production in the sea. Journal du Conseil 18: 117–140.CrossRefGoogle Scholar
  74. Nigro, L.M., and G.M. King. 2007. Disparate distributions of chemolithotrophs containing form IA or IC large subunit genes for ribulose-1,5-bisphosphate carboxylase/oxygenase in intertidal marine and littoral lake sediments. FEMS Microbiology Ecology 60: 113–125.CrossRefGoogle Scholar
  75. Nittrouer, C.A., T.B. Curtin, and D.J. Demaster. 1986. Concentration and flux of suspended sediment on the Amazon Continental-Shelf. Continental Shelf Research 6: 151–174.CrossRefGoogle Scholar
  76. Okano, Y., K.R. Hristova, C.M. Leutenegger, L.E. Jackson, R.F. Denison, B. Gebreyesus, D. Lebauer, and K.M. Scow. 2004. Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Applied and Environmental Microbiology 70: 1008–1016.CrossRefGoogle Scholar
  77. Perez, R.C., and A. Matin. 1982. Carbon dioxide assimilation by Thiobacillus novellus under nutrient-limited mixotrophic conditions. Journal of Bacteriology 150: 46–51.Google Scholar
  78. Roegner, G.C., J.A. Needoba, and A.M. Baptista. 2011. Coastal upwelling supplies oxygen-depleted water to the Columbia River estuary. PLoS One 6.Google Scholar
  79. Schippers, A., D. Kock, C. Höft, G. Köweker, and M. Siegert. 2012. Quantification of microbial communities in subsurface marine sediments of the Black Sea and off Namibia. Frontiers in Microbiology 3: 16. doi:10.3389/fmicb.2012.00016.CrossRefGoogle Scholar
  80. Schloss, P.D., and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71: 1501–1506.CrossRefGoogle Scholar
  81. Schubel, J.R. 1968. Turbidity maximum of northern Chesapeake Bay. Science 161: 1013.CrossRefGoogle Scholar
  82. Selesi, D., M. Schmid, and A. Hartmann. 2005. Diversity of green-like and red-like ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes (cbbL) in differently managed agricultural soils. Applied and Environmental Microbiology 71: 175–184.CrossRefGoogle Scholar
  83. Selesi, D., I. Pattis, M. Schmid, E. Kandeler, and A. Hartmann. 2007. Quantification of bacterial RubisCO genes in soils by cbbL targeted real-time PCR. Journal of Microbiological Methods 69: 497–503.CrossRefGoogle Scholar
  84. Shively, J.M., G. van Keulen, and W.G. Meijer. 1998. Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annual Review of Microbiology 52: 191–230.CrossRefGoogle Scholar
  85. Small, L.F., and F.G. Prahl. 2004. A particle conveyor belt process in the Columbia River estuary: evidence from chlorophyll a and particulate organic carbon. Estuaries 27: 999–1013.CrossRefGoogle Scholar
  86. Smith, M.W., L. Herfort, K. Tyrol, D. Suciu, V. Campbell, B.C. Crump, T.D. Peterson, P. Zuber, A.M. Baptista, and H.M. Simon. 2010. Seasonal changes in bacterial and archaeal gene expression patterns across salinity gradients in the Columbia River coastal margin. PLoS One 5: e13312.CrossRefGoogle Scholar
  87. Sogin, M.L., H.G. Morrison, J.A. Huber, D.M. Welch, S.M. Huse, P.R. Neal, J.M. Arrieta, and G.J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences 103: 12115–12120.CrossRefGoogle Scholar
  88. Sorokin, Y.I. 1972. The bacterial population and the processes of hydrogen sulphide oxidation in the Black Sea. Journal du Conseil 34: 423–454.CrossRefGoogle Scholar
  89. Swingley, W.D., S. Sadekar, S.D. Mastrian, et al. 2007. The complete genome sequence of Roseobacter denitrificans reveals a mixotrophic rather than photosynthetic metabolism. Journal of Bacteriology 189: 683–690.CrossRefGoogle Scholar
  90. Taylor, G.T., M. Iabichella-Armas, R. Varela, F. Müller-Karger, X. Lin, and M.I. Scranton. 2006. Microbial ecology of the Cariaco Basin’s redoxcline: the US–Venezuela Cariaco times series program. Past and Present Water Column Anoxia 64: 471–499.CrossRefGoogle Scholar
  91. Taylor, G.T., M. Iabichella, T.Y. Ho, M.I. Scranton, R.C. Thunell, F. Muller-Karger, and R. Varela. 2001. Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnology and Oceanography 46: 148–163.CrossRefGoogle Scholar
  92. Tebo, B.M., H.A. Johnson, J.K. McCarthy, and A.S. Templeton. 2005. Geomicrobiology of manganese(II) oxidation. Trends in Microbiology 13: 421–428.CrossRefGoogle Scholar
  93. Tolli, J., and G.M. King. 2005. Diversity and structure of bacterial chemolithotrophic communities in pine forest and agroecosystem soils. Applied and Environmental Microbiology 71: 8411–8418.CrossRefGoogle Scholar
  94. Tuttle, J.H., and H.W. Jannasch. 1977. Thiosulfate stimulation of microbial dark stimulation of carbon dioxide in shallow marine waters. Microbial Ecology 4: 9–25.CrossRefGoogle Scholar
  95. Uncles, R.J., R.J.M. Howland, A.E. Easton, M.L. Griffiths, C. Harris, R.S. King, A.W. Morris, D.H. Plummer, and E.M.S. Woodward. 1998. Seasonal variability of dissolved nutrients in the Humber-Ouse Estuary, UK. Marine Pollution Bulletin 37: 234–246.CrossRefGoogle Scholar
  96. Videmšek, U., A. Hagn, M. Suhadolc, V. Radl, H. Knicker, M. Schloter, and D. Vodnik. 2009. Abundance and diversity of CO2-fixing bacteria in grassland soils close to natural carbon dioxide springs. Microbial Ecology 58: 1–9.CrossRefGoogle Scholar
  97. Whitman, W.B., D.C. Coleman, and W.J. Wiebe. 1998. Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences 95: 6578–6583.CrossRefGoogle Scholar
  98. Yuan, H.,T. Ge, C. Chen, A. G. O'Donnell, and J. Wu 2012. Significant role for microbial autotrophy in the sequestration of soil carbon. Applied and Environmental Microbiology 78:2328–2336.Google Scholar
  99. Zhang, Y.L., and A.M. Baptista. 2008. SELFE: a semi-implicit Eulerian–Lagrangian finite-element model for cross-scale ocean circulation. Ocean Modelling 21: 71–96.CrossRefGoogle Scholar
  100. Zhang, Y.L., A.M. Baptista, and E.P. Myers. 2004. A cross-scale model for 3D baroclinic circulation in estuary–plume–shelf systems: I. Formulation and skill assessment. Continental Shelf Research 24: 2187–2214.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2013

Authors and Affiliations

  • S. L. Bräuer
    • 1
    • 2
  • K. Kranzler
    • 2
  • N. Goodson
    • 1
  • D. Murphy
    • 2
  • H. M. Simon
    • 2
  • A. M. Baptista
    • 2
  • B. M. Tebo
    • 2
  1. 1.Department of BiologyAppalachian State UniversityBooneUSA
  2. 2.Center for Coastal Margin Observation & Prediction and Division of Environmental & Biomolecular SystemsOregon Health & Science UniversityBeavertonUSA

Personalised recommendations