Response of Estuarine Biofilm Microbial Community Development to Changes in Dissolved Oxygen and Nutrient Concentrations
- 284 Downloads
The information content and responsiveness of microbial biofilm community structure, as an integrative indicator of water quality, was assessed against short-term changes in oxygen and nutrient loading in an open-water estuarine setting. Biofilms were grown for 7-day periods on artificial substrates in the Pensacola Bay estuary, Florida, in the vicinity of a wastewater treatment plant (WWTP) outfall and a nearby reference site. Substrates were deployed floating at the surface and near the benthos in 5.4 m of water. Three sampling events covered a 1-month period coincident with declining seasonal WWTP flow and increasing dissolved oxygen (DO) levels in the bottom waters. Biomass accumulation in benthic biofilms appeared to be controlled by oxygen rather than nutrients. The overriding effect of DO was also seen in DNA fingerprints of community structure by terminal restriction fragment length polymorphism (T-RFLP) of amplified 16S rRNA genes. Ribotype diversity in benthic biofilms at both sites dramatically increased during the transition from hypoxic to normoxic. Terminal restriction fragment length polymorphism patterns showed pronounced differences between benthic and surface biofilm communities from the same site in terms of signal type, strength, and diversity, but minor differences between sites. Sequencing of 16S rRNA gene clone libraries from benthic biofilms at the WWTP site suggested that low DO levels favored sulfate-reducing prokaryotes (SRP), which decreased with rising oxygen levels and increasing overall diversity. A 91-bp ribotype in the CfoI-restricted 16S rRNA gene T-RFLP profiles, indicative of SRP, tracked the decrease in relative SRP abundance over time.
KeywordsTerminal Restriction Fragment Length Polymorphism Oyster Reef Restriction Fragment Length Polymorphism Pattern Terminal Restriction Fragment Length Polymorphism Profile Terminal Restriction Fragment Length Polymorphism Pattern
We thank Jeff Alison, Laura Pennington, Natasha Rondon, and Matt Wagner for their field assistance and Melissa Hagy for the data management.
This research was supported by a grant from the U.S. Environmental Protection Agency (US EPA)’s Science to Achieve Results (STAR) Estuarine and Great Lakes (EaGLe) Coastal Initiative through funding to the CEER-GOM Project, US EPA Agreement EPA/R-8294580.
- 2.Balba, MT, Nedwell, DB (1982) Microbial metabolism of acetate, propionate and butyrate in anoxic sediments from the Colne Point saltmarsh, Essex, UK. J Gen Microbiol 128: 1415–1422Google Scholar
- 3.Bordenave, S, Fourçans, A, Blanchard S, Goñi, MS, Caumette, P, Duran, R (2004) Structure and functional analyses of bacterial communities changes in microbial mats following petroleum exposure. Ophelia 58: 195–204Google Scholar
- 5.Brigmon, RL, Martin, HW, Morris, TL, Britton, G, Zam, SG (1994) Biogeochemical ecology of Thiothrix spp. in underwater limestone caves. Geomicrobiol J 12: 141–159Google Scholar
- 13.Eaton, AD, Clesceri, LS, Greenberg, AE (1995) Standard Methods for the Examination of Water and Wastewater, 19th edn. American Public Health Association; American Water Works Association; Water Environment Federation, Washington, D.C.Google Scholar
- 15.Fenchel, T (1969) The ecology of marine microbenthos IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna communities with special reference to the ciliated Protozoa. Ophelia 6: 1–182Google Scholar
- 20.Johnson, MA, Diouris, M, Le Pennec, M (1994) Endosymbiotic bacterial contribution in the carbon nutrition of Loripes lucinalis (Mollusca: Bivalvia). Symbiosis 17: 1–13Google Scholar
- 22.Lane, DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt, E, Goodfellow, M (Eds.) Nucleic Acid Techniques in Bacterial Systematics, John Wiley & Sons, Chichester, United Kingdom, pp 115–175Google Scholar
- 25.McCune, B, Mefford, MJ (1999) PC-ORD: Multivariate Analysis of Ecological Data. MjM Software Design, Gleneden Beach, Oregon, USAGoogle Scholar
- 26.Minz, D, Fishbain, S, Green, SJ, Muyzer, G, Cohen, Y, Rittmann, BE, Stahl, DA (1999) Unexpected population distribution in a microbial mat community: sulfate-reducing bacteria localized to the highly oxic chemocline in contrast to a eukaryotic preference for anoxia. Appl Environ Microbiol 65: 4659–4665PubMedGoogle Scholar
- 27.Minz, D, Flax, JL, Green, SJ, Muyzer, G, Cohen, Y, Wagner, M, Rittmann, BE, Stahl, DA (1999) Diversity of sulfate-reducing bacteria in oxic and anoxic regions of a microbial mat characterized by comparative analysis of dissimilatory sulfite reductase genes. Appl Environ Microbiol 65: 4666–4671PubMedGoogle Scholar
- 29.Navarrete, A, Urmenta, J, Cantu, JM, Vegas, E, White, DC, Guerrero, R (2004) Signature lipid biomarkers of microbial mats of the Ebro Delta (Spain), Camargue and Étang (France): an assessment of biomass and activity. Ophelia 58: 175–188Google Scholar
- 30.Nelson, DC, Fisher, CR (1995) Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps. In: Karl, DM (Ed.) The Microbiology of Deep-Sea Hydrothermal Vents, CRC Press, Boca Raton, FL, pp 125–167Google Scholar
- 38.Rinke, C, Schmitz-Esser, S, Stoecker, K, Nussbaumer, AD, Molnár, DA, Vanura, Wagner, KM, Horn, M, Ott, JA, Brigh, M (2006) “Candidatus Thiobios zoothamnicoli,” an ectosymbiotic bacterium covering the giant marine ciliate Zoothamnium niveum. Appl Environ Microbiol 72: 2014–2021PubMedCrossRefGoogle Scholar
- 39.Röling, WFM, Milner, MG, Martin Jones, D, Fratepietro, F, Swannell, RPJ, Daniel, F, Head, IM (2004) Bacterial community dynamics and hydrocarbon degradation during a field-scale evaluation of bioremediation on a mudflat beach contaminated with buried oil. Appl Environ Microbiol 70: 2603–2613PubMedCrossRefGoogle Scholar
- 43.Sievert, SM, Heidorn, T, Kuever, J (2000) Halothiobacillus kellyi sp. nov., a mesophilic, obligately chemolithoautotrophic, sulfur-oxidizing bacterium isolated from a shallow-water hydrothermal vent in the Aegean sea, and emended description of the genus Halothiobacillus. Int J Syst Evol Microbiol 50: 1229–1237PubMedGoogle Scholar
- 44.Snyder, RA, Lewis, MA, Nocker, A, Lepo, JE (2004) Microbial biofilms as integrative sensors of environmental quality. In: Bortone, SA (Ed.) Estuarine Indicators, CRC Press, Boca Raton, FL, pp 111–126Google Scholar
- 46.U.S. Environmental Protection Agency (1997) Revision to Rapid Bioassessment Protocols for Use in Streams and Rivers: Periphyton, Benthic Macroinvertebrates, and Fish. EPA 841-D-97-002. United States Environmental Protection Agency, Washington, D.C.Google Scholar
- 47.Widdel, F, Bak, F (1992) Gram-negative mesophilic sulfate-reducing bacteria. In: Balows, A, Trüper, HG, Dworkin, M, Harder, W, Schleifer, K-H (Eds.) The Procaryotes: A Handbook on the Biology of Bacteria: Ecophysiology, Identification, Application, Springer-Verlag, NYGoogle Scholar