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Seasonal oscillation of microbial iron and sulfate reduction in saltmarsh sediments (Sapelo Island, GA, USA)

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Abstract

Seasonal variations in anaerobic respiration pathways were investigated at three saltmarsh sites using chemical data, sulfate reduction rate measurements, enumerations of culturable populations of anaerobic iron-reducing bacteria (FeRB), and quantification of in situ 16S rRNA hybridization signals targeted for sulfate-reducing bacteria (SRB). Bacterial sulfate reduction in the sediments followed seasonal changes in temperature and primary production of the saltmarsh, with activity levels lowest in winter and highest in summer. In contrast, a dramatic decrease in the FeRB population size was observed during summer at all sites. The collapse of FeRB populations during summer was ascribed to high rates of sulfide production by SRB, resulting in abiotic reduction of bioavailable Fe(III) (hydr)oxides. To test this hypothesis, sediment slurry incubations at 10, 20 and 30 °C were carried out. Increases in temperature and labile organic carbon availability (acetate or lactate additions) increased rates of sulfate reduction while decreasing the abundance of culturable anaerobic FeRB. These trends were not reversed by the addition of amorphous Fe(III) (hydr)oxides to the slurries. However, when sulfate reduction was inhibited by molybdate, no decline in FeRB growth was observed with increasing temperature. Addition of dissolved sulfide adversely impacted propagation of FeRB whether molybdate was added or not. Both field and laboratory data therefore support a sulfide-mediated limitation of microbial iron respiration by SRB. When total sediment respiration rates reach their highest levels during summer, SRB force a decline in the FeRB populations. As sulfate reduction activity slows down after the summer, the FeRB are able to recover.

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References

  • Aller R.C. 2001. Transport and reactions in the bioirrigated zone. In: Boudreau B.P. and Jørgensen B.B. (eds), The Benthic Boundary Layer: Transport Processes and Biogeochemistry. Oxford University Press, Southampton, pp. 269–301.

    Google Scholar 

  • Aller R.C. and Rude P.D. 1988. Complete oxidation of solid phase sulfides by manganese and bacteria in anoxic marine sediments. Geochimica et Cosmochimica Acta 52: 751–765.

    Google Scholar 

  • Alongi D.M. 1997. Coastal ecosystem processes. CRC Press, Boca Raton, FL, USA.

    Google Scholar 

  • Amann R.I., Krumholz L. and Stahl D.A. 1990. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. Journal of Bacteriology 172: 762–770.

    Google Scholar 

  • Amann R.I., Stromley J., Devereux R., Key R. and Stahl D.A. 1992. Molecular and microscopic identification of sulfate-reducing bacteria in multispecies biofilms. Applied and Environmental Microbiology 58: 614–623.

    Google Scholar 

  • Amann R., Glockner F.O. and Neef A. 1997. Modern methods in subsurface microbiology: in situ identication of microorganisms with nucleic acid probes. FEMS Microbiology Reviews 20: 191–200.

    Google Scholar 

  • Berner R.A. 1964. Iron sulfides formed from aqueous solution at low temperatures and atmospheric pressure. Journal of Geology 72: 299–306.

    Google Scholar 

  • Berner R.A. 1980. Early Diagenesis. Princeton University Press, Princeton, NJ, USA.

    Google Scholar 

  • Brandes J.A. and Devol A.H. 1995. Simultaneous nitrate and oxygen respiration in coastal sediments: evidence for discrete diagenesis. Journal of Marine Research 53: 771–797.

    Google Scholar 

  • Burdige D.J. 1993. The biogeochemistry of manganese and iron reduction in marine sediments. Earth-Science Reviews 35: 249–284.

    Google Scholar 

  • Burdige D.J. and Nealson K.H. 1986. Chemical and microbiological studies of sulfide-mediated manganese reduction. Geomicrobiology Journal 4: 361–387.

    Google Scholar 

  • Burnes B., Mulberry M. and DiChristina T. 1998. Design and application of two rapid screening techiniques for the isolation of Mn(IV) reduction-deficient mutants. Applied and Environmental Microbiology 64: 2716–2720.

    Google Scholar 

  • Canfield D.E. 1993. Organic matter oxidation in marine sediments. In: Wollast R., Mackenzie F.T. and Chou L. (eds), Interactions of C, N, P and S Biogeochemical Cycles and Global Change, NATO ASI Series. Springer-Verlag, Berlin, pp. 333–363.

    Google Scholar 

  • Canfield D.E. and Des Marais D.J. 1991. Aerobic sulfate reduction in microbial mats. Science 251: 1471–1473.

    Google Scholar 

  • Canfield D.E. and Des Marais D.J. 1993. Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochimica et Cosmochimica Acta 57: 3971–3984.

    Google Scholar 

  • Canfield D.E., Jørgensen B.B., Fossing H., Glud R., Gundersen J., Ramsing N.B. et al. 1993. Pathways of organic carbon oxidation in three continental margin sediments. Marine Geology 113: 27–40.

    Google Scholar 

  • Dai T. and Wiegert R.G. 1996. Ramet population dynamics and net aerial primary productivity of Spartina alterniflora. Ecology 77: 276–288.

    Google Scholar 

  • Dame R.F. and Kenny P.D. 1986. Variability of Spartina alterniflora primary production in the euhaline North Inlet estuary. Marine Ecology Progress Series 32: 71–80.

  • Devereux R., Kane M.D., Winfrey J. and Stahl D.A. 1992. Genus-and group-specific hybridization probes for determinative and environmental studies of sulfate-reducing bacteria. Systematic and Applied Microbiology 15: 601–609.

    Google Scholar 

  • DiChristina T.J. and DeLong E.F. 1994. Isolation of anaerobic respiratory mutants of Shewanella putrefaciens and genetic analysis of mutants deficient in anerobic growth on Fe+3. Journal of Bacteriology 176: 1468–1474.

    Google Scholar 

  • Elsgaard L. and Jørgensen B.B. 1992. Anoxic transformations of radiolabeled hydrogen sulfide in marine and freshwater sediments. Geochimica et Cosmochimica Acta 56: 2425–2435.

    Google Scholar 

  • Froelich P.N., Klinkhammer G.P., Bender M.L., Luedtke N.A., Heath G.R., Cullen D. et al. 1979. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochimica et Cosmochimica Acta 43: 1075–1090.

    Google Scholar 

  • Goldhaber M.B. and Kaplan I.R. 1974. The sulfur cycle. In: Goldberg E.D. (ed.), The Sea. John Wiley and Sons, Inc., New York, pp. 569–655.

    Google Scholar 

  • Grasshoff K., Ehrhardt M. and Kremling K. (eds) 1982. Methods of Seawater Analysis. Verlag Chemie, Germany, 419 pp.

    Google Scholar 

  • Greenberg A.E., Clesceri L.S. and Eaton A.D. (eds) 1992. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC, USA.

    Google Scholar 

  • von Gunten U. and Furrer G. 2000. Steady-state modeling of biogeochemical processes in columns with aquifer material: 2. Dynamics of iron-sulfur interactions. Chemical Geology 167: 271–284.

    Google Scholar 

  • Hesslein R.H. 1976. An in situ sampler for close interval pore water studies. Limnology and Oceanography 21: 912–914.

    Google Scholar 

  • Hines 1991. The role of certain infauna and vascular plants in the mediation of redox reactions in marine sediments. In: Berthelin J. (ed.), Diversity of Environmental Biogeochemistry. Elsevier, pp. 275–286.

  • Hines M.E., Knollmeyer S.L. and Tugel J.B. 1989. Sulfate reduction and other sedimentary biogeochemistry in a northern New England salt marsh. Limnology and Oceanography 34: 578–590.

    Google Scholar 

  • Hines M.E., Evans R.S., Genthner B.R., Sharak W., Friedman S., Rooney-Varga J.N. et al. 1999. Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. Applied Environmental Microbiology 65: 2209–2216.

    Google Scholar 

  • Hoehler T.M., Alperin M.J., Albert D.B. and Martens C.S. 1998. Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochimica et Cosmochimica Acta 62: 1745–1756.

    Google Scholar 

  • Holmer M. and Nielsen S.L. 1997. Sediment sulfur dynamics related to biomass-density patterns in Zostera marina (eelgrass) beds. Marine Ecology Progress Series 146: 163–171.

  • Howarth R.W. and Teal J.M. 1979. Sulfate reduction in a New England salt marsh. Limnology and Oceanography 24: 999–1013.

    Google Scholar 

  • Howarth R.W. and Hobbie J.E. 1982. The regulation of decomposition and heterotrophic microbial activity in salt marsh soils: a review. In: Kennedy V.S. (ed.), Estuarine Comparisons. Academic Press, pp. 183–207.

  • Howarth R.W. and Giblin A. 1983. Sulfate reduction in the salt marshes at Sapelo Island, Georgia. Limnology and Oceanography 28: 70–82.

    Google Scholar 

  • Howarth R.W. and Merkel S. 1984. Pyrite formation and the measurement of sulfate reduction in salt marsh sediments. Limnology and Oceanography 29: 598–608.

    Google Scholar 

  • Howes B.L., Dacey J.W. and King G.M. 1984. Carbon flow through oxygen and sulfate reduction pathways in salt marsh sediments. Limnology and Oceanography 29: 1037–1051.

    Google Scholar 

  • Isaksen M.F. and Finster K. 1996. Sulphate reduction in the root zone of the seagrass Zostera noltii on the intertidal flats of a coastal lagoon (Arcachon, France). Marine Ecology Progress Series 137: 187–194.

  • Jacobson M.E. 1994. Chemical and biological mobilization of Fe(III) in marsh sediments. Biogeochemistry 25: 41–60.

    Google Scholar 

  • Jørgensen B.B. 1990. A thiosulfate shunt in the sulfur cycle of marine sediments. Science 249: 152–154.

    Google Scholar 

  • Jørgensen B.B. and Bak F. 1991. Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). Applied and Environmental Microbiology 57: 847–856.

    Google Scholar 

  • King G.M. 1988. Patterns of sulfate reduction and the sulfur cycle in a South Carolina salt marsh. Limnology and Oceanography 33: 376–390.

    Google Scholar 

  • King G.M., Klug M.J., Wiegert R.G. and Chalmers A.G. 1982. Relation of soil water movement and sulfide concentration to Spartina alterniflora production in a Georgian salt marsh. Science 218: 61–63.

    Google Scholar 

  • Koretsky C.M., Meile C. and Van Cappellen P. 2002. Quantifying bioirrigation using ecological parameters: a stochastic approach. Geochemical Transactions 3: 17–30.

    Google Scholar 

  • Koretsky C.M., Van Cappellen P., DiChristina T.J., Kostka J., Lowe K., Moore C. et al. Contrasting geochemical and microbial structures of saltmarsh sediments: Seasonal and spatial trends at Sapelo Island (Georgia, USA).

  • Koroleff F. 1983. Determination of trace metals. In: Grasshoff K., Ehrhardt M. and Kremling K. (eds), Methods of Seawater Analysis. Verlag Chemie, pp. 189–246.

  • Kostka J.E. and Luther G.W. 1994. Partitioning and speciation of solid phase iron in saltmarsh sediments. Geochimica et Cosmochimica Acta, April 1994, V58, N7.

  • Kostka J.E., Gribsholt B., Petrie E., Dalton D., Skelton H. and Kristensen E. 2002a. The rates and pathways of carbon oxidation in bioturbated saltmarsh sediments. Limnology and Oceanography 47: 230–240.

    Google Scholar 

  • Kostka J.E., Roychoudhury A. and Van Cappellen P. 2002b. Rates and controls of anaerobic microbial respiration across spatial and temporal gradients in saltmarsh sediments. Biogeochemistry 50: 49–76.

    Google Scholar 

  • Lovley D.R. and Klug M.J. 1986. Model for the distribution of sulfate reduction and methanogenesis in freshwater sediments. Geochimica et Cosmochimica Acta 50: 11–18.

    Google Scholar 

  • Lovley D.R. and Phillips E.J.P. 1986. Availability of ferric iron for microbial reduction in bottom sediments of the freshwater tidal Potomac River. Applied and Environmental Microbiology 52: 751–757.

    Google Scholar 

  • Lovley D.R. and Phillips E.J.P. 1987. Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Applied and Environmental Microbiology 53: 2636–2641.

    Google Scholar 

  • Lowe K., DiChristina T.J., Roychoudhury A. and Van Cappellen P. 2000. Microbiological and geochemical characterization of microbial Fe(III) reduction in salt marsh sediments. Geomicrobiology Journal 17: 163–178.

    Google Scholar 

  • Luna G.M., Manini E. and Danovaro R. 2002. Large fraction of dead and inactive bacteria in coastal marine sediments: comparison of protocols for determination and ecological significance. Applied and Environmental Microbiology 68: 3509–3513.

    Google Scholar 

  • Meile C., Koretsky C. and Van Cappellen P. 2001. Quantifying bioirrigation in aquatic sediments: an inverse modeling approach. Limnology and Oceanography 46: 164–177.

    Google Scholar 

  • Moran M.A., Torsvik T.L., Torsvik T. and Hodson R.E. 1993. Direct extraction and purification of rRNA for ecological studies. Applied and Environmental Microbiology 59: 915–918.

    Google Scholar 

  • Myers C.R. and Nealson K.H. 1988. Bacterial manganese reduction and growth with manganese oxide as sole terminal electron acceptor. Science 240: 1319–1321.

    Google Scholar 

  • Pace N.R., Stahl D.R., Lane D.J. and Olsen G.J. 1986. The analysis of natural populations by ribosomal RNA sequence. Advances in Microbiology and Ecology 9: 1–55.

    Google Scholar 

  • Peiffer S., Dos Santos Afonso M., Wehrli B. and Gächter R. 1992. Kinetics and mechanism of the reaction of H2S with lepidocrocite. Environmental Science and Technology 26: 2408–2413.

    Google Scholar 

  • Pomeroy L.R., Darley W.M., Dunn E.L., Gallagher J.L., Haines E.B. and Whitney D.M. 1981. Primary production. In: Pomeroy L.R. and Wiegert R.G. (eds), The Ecology of a Salt Marsh. Springer, New York, pp. 39–67.

    Google Scholar 

  • Pyzik A.J. and Sommer S.E. 1981. Sedimentary iron monosulfides: kinetics and mechanism of formation. Geochimica et Cosmochimica Acta 45: 687–698.

    Google Scholar 

  • dos Santos Afonso M. and Stumm W. 1992. Reductive dissolution of iron III (hydr)oxides by hydrogensulfide. Langmuir 8: 1671–1675.

    Google Scholar 

  • Sarazin G., Michard G. and Prevot F. 1998. A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples. Water Research 33: 290–294.

    Google Scholar 

  • Schubauer J.P. and Hopkinson C.S. 1984. Above-and belowground emergent macrophyte production and turnover in a coastal marsh ecosystem, Georgia. Limnology and Oceanography 29: 1052–1065.

    Google Scholar 

  • Schwertmann U. and Cornell R.M. 2000. Iron Oxides in the Laboratory: Preparation and Characterization. Wiley-VCH, New York.

    Google Scholar 

  • Sørensen J. 1982. Reduction of ferric iron in anaerobic, marine sediment and interaction with reduction of nitrate and sulfate. Applied and Environmental Microbiology 43: 319–324.

    Google Scholar 

  • Stephen J.R., McCaig A.E., Smith Z., Prosser J.I. and Embley T.M. 1996. Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Applied and Environmental Microbiology 62: 4147–4154.

    Google Scholar 

  • Tabatabai M.A. 1974. A rapid method for determination of sulfate in water samples. Environmental Letters 7: 237–243.

    Google Scholar 

  • Thamdrup B., Fossing H. and Jørgensen B.B. 1994. Manganese, iron, and sulfur cycling in a coastal marine sediment, Aarhus Bay, Denmark. Geochimica et Cosmochimica Acta 58: 5115–5129.

    Google Scholar 

  • Thamdrup 2000. Bacterial manganese and iron reduction in aquatic sediments. Advances in Microbial Ecology 16: 41–84.

    Google Scholar 

  • Thamdrup B. and Canfield D.E. 2000. Benthic respiration in aquatic sediments. In: Sala O.E. (ed.), Methods in Ecosystem Science. Springer, pp. 86–103.

  • Urban N.R., Brezonik P.L., Baker L.A. and Sherman L.A. 1994. Sulfate reduction and diffusion in sediments of Little Rock Lake, Wisconsin. Limnology and Oceanography 39: 797–815.

    Google Scholar 

  • Van Cappellen P. and Wang Y. 1996. Cycling of iron and manganese in surface sediments: a general theory for the coupled transport and reaction of carbon, oxygen, nitrogen, sulfur, iron, and manganese. American Journal of Science 296: 197–243.

    Google Scholar 

  • Viollier E., Inglett P.W., Hunter K., Roychoudhury A.N. and Van Cappellen P. 2000. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Applied Geochemistry 15: 785–790.

    Google Scholar 

  • Wang Y. and Van Cappellen P. 1996. A multicomponent reactive transport model of early diagenesis: Application to redox cycling in coastal marine sediments. Geochimica et Cosmochimica Acta 60: 2993–3014.

    Google Scholar 

  • Ward D.M., Ferris F.J., Nold S.C. and Bateson M.M. 1998. A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiology and Molecular Biology Reviews 62: 1353–1370.

    Google Scholar 

  • Yao W. and Millero F.J. 1996. Oxidation of hydrogen sulfide by hydrous Fe(III) oxides in seawater. Marine Chemistry 52: 1–16.

    Google Scholar 

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Authors
  1. Carla M. Koretsky
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  2. Charles M. Moore
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  3. Kristine L. Lowe
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  4. Christof Meile
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Koretsky, C.M., Moore, C.M., Lowe, K.L. et al. Seasonal oscillation of microbial iron and sulfate reduction in saltmarsh sediments (Sapelo Island, GA, USA). Biogeochemistry 64, 179–203 (2003). https://doi.org/10.1023/A:1024940132078

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