Abstract
Aspects of denitrification and benzoate degradation were studied in two estuarine microbial mat communities on the California coast by measuring the depth distributions of potential denitrification rates, genetic potential for denitrification, nitrate concentration, benzoate mineralization rates, total bacterial abundance, and abundance of a denitrifying strain (TBD-8b) isolated from one of the sites. Potential denitrification was detected in microbial mat cores from both Elkhorn Slough and Tomales Bay. Maximum denitrification rates were more than two orders of magnitude higher at Elkhorn Slough (3.14 mmol N m−2 d−1) than at Tomales Bay (0.02 mmol N m−2 d−1), and at both sites, the maximum rates occurred in the 0–2 mm depth interval. Ambient pore [NO3+NO2] was substantially higher at Elkhorn Slough than at Tomales Bay. Incorporation and mineralization of benzoate was maximal near the mat surface at Elkhorn Slough. The areal rate of benzoate utilization was 1045 nmol C m−2 d−1, which represented utilization of 70% of the added substrate in 24 h. Total bacterial and TBD-8b abundances were greatest near the surface at both Tomales Bay and Elkhorn Slough, and TBD-8b represented less than 0.2% of the total. Genetic potential for denitrification, quantified by hybridization with a nitrite reductase gene fragment, was present below the mat surface at average levels representing presence of the gene in approximately 10% of the total cells.
Similar content being viewed by others
References
ABA Consultants (1989) Elkhorn Slough wetland management plan. ABA Consultants, Environmental research, assessment and planning Capitola, CA
Atlas RM (1981) Microbial degradation of petroleum hydrocarbons: An environmental perspective. Microbiol Rev 45:180–209
Bauld J (1984) Microbial mats in marginal marine environments: Shark Bay, Western Australia and Spencer Gulf, South Australia. In: Cohen Y, Castenholz R, Halvorson H (eds) Microbial Mats: Stromatolites. Alan R Liss, New York, pp 39–58
Bossert I, Bartha R (1984) The fate of petroleum in soil ecosystems In: Atlas RM (ed) Petroleum Microbiology. Macmillan, New York pp 434–476
Caffrey JM, Shaw S, Silberstein M, De Vogelaere A, White M, (1997) Water quality monitoring in Elkhon Slough: A summary result 1988–1996. A report to Elkhorn Slough National Estuarine Research Reserve.
Canfield DE, Des Marais DJ (1993) Biogeochemical cycles of carbon, sulfur and free oxygen in a microbial mat. Geochim Cosmochim Acta 57:3971–3984
Carlucci AF, Pramer D (1957) Factors influencing the plate method for determining abundance of bacteria in sea water. Proc Soc Exp Biol Med 96:392–394
Chaudhry GR, Chapalamadugu S (1991) Biodegradation of halogenated organic compounds. Microbiol Rev 55:59–79
Cohen Y, Castenholz R, Halvorson H (1984) The interdisciplinary approach to the study of microbial mats: Perspectives for future research discussion. In: Cohen Y, Castenholz R, Halvorson H (eds) Microbial Mats: Stromatolites. Alan R Liss, New York pp 471–477
Cohen Y, Rosenberg E (1989) Microbial mats: Physiological ecology of benthic microbial communities. Amer Soc Microbiol, Washington, DC, 494 pp.
Craven DB, Jahnke RA, Carlucci AF (1986) Fine-scale vertical distributions of microbial biomas and activity in California Borderland sediments. Deep-Sea Res 33:379–390
Dahle AB, Laake M (1982) Diversity dynamics of marine bacteria studied by immunofluorescent staining on membrane filters. Appl Environ Microb 43:169–176
Daugherty DD, Karel SF (1994) Degradation of 2,4-dichlorophenoxyacetic acid by Pseudomonas cepacia DBO1 (pRO101) in a dual-substrate chemostat. Appl Environ Microbiol 60:3261–3267
Evans PJ, Mang DT, Kim KS, Young LY (1991) Anaerobic degradation of toluene by a denitrifying bacterium. Appl Environ Microbiol 57:1139–1145
Francis CA, Francis AK, Golet DS, Ward BB (1998) Quantification of catechol 2,3-dioxygenase gene homology abundance in intertidal sediments. Aq Microb Ecol 15:225–231
Galli E (1994) The role of microorganisms in environmental decontamination. In: Renzoni A, Mattei N, Lari L, Fossi M (eds) Contaminants in the Environment: A Multidisciplinary Assessment of Risks to Man and Other Organisms. CRC Press, Inc, Boca Raton, FL, pp 235–246
Guo C, Sun W, Harsh JB, Ogram A (1997) Hybridization analysis of microbial DNA from fuel oil-contaminated and noncontaminated soil. Microb Ecol 34:178–187 DOI: 10.1007/s002489900047
Herbes SE, Schwall LR (1978) Microbial transformation of polycyclic aromatic hydrocarbons in pristine and petroleum-contaminated sediments. Appl Environ Microbiol 35:306–316
Hogan ME, Ward BB (1998) Response of a marine sediment microbial community exposed to 2,4-dichlorophenoxyacetic acid. Microb Ecol 35:72–82 DOI: 10.1007/s002489900061
Jensen K, Sloth NP, Risgaard-Petersen N, Rysgaard S, Revsbech NP (1994) Estimation of nitrification and denitrification from in microprofiles of oxygen and nitrate in model sediment systems. Appl Environ Microbiol 60:2094–2100
Jones M (1984) Nitrate reduction by shaking with cadmium: Alternative to cadmium columns. Water Res 18:643–646
Joye SB, Paerl HW (1993a) Contemporaneous nitrogen fixation and denitrification in intertidal microbial mats: Rapid response to runoff events. Mar Ecol Prog Ser 94:267–274
Joye SB, Paerl HW (1993b) Nitrogen fixation and denitrification in the intertidal and subtidal environments of Tomales Bay, California. In: Oremland RS (ed) The Biogeochemistry of Global Change: Radiative Trace Gases. Blackwell Scientific, New York, pp 633–653
Joye SB, Paerl HW (1994) Nitrogen cycling in microbial mats: Rates and patterns of denitrification and nitrogen fixation. Mar Biol 119:285–295
Kerkhof L (1991) A comparison of substrates for quantifying the signal from a nonradiolabeled DNA probe. Anal Biochem 205:359–364
Kuhn EP, Zeyer J, Eicher P, Schwarzenbach RP (1988) Anaerobic degradation of alkylated benzenes in denitrifying laboratory aquifer columns. Appl Environ Microbiol 54:490–496
Largier JL, Hollibaugh JT, Smith SV (1997) Seasonally hypersaline estuaries in Mediterranean-climate regions. Est Coast Shelf Sci 45:789–797
Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315
Leahy JG, Somerville CC, Cunningham KA, Adamantiades GA, Byrd JJ, Colwell RR (1990) Hydrocarbon mineralization in sediments and plasmid incidence in sediment bacteria from the Campeche Bank. Appl Environ Microb 56:1565–1570
Michelcic JR, Luthy RG (1988a) Degradation of polycyclic aromatic hydrocarbon compounds under various redox conditions in soil-water systems. Appl Environ Microbiol 54:1182–1187
Michelcic JR, Luthy RG (1988b) Microbial degradation of acenaphthene and naphthalene under denitrification conditions in soil-water systems. Appl Environ Microbiol 54:1188–1198
Miller LG, Oremland RS, Paulsen S (1986) Measurement of nitrous oxide reductase activity in aquatic sediments. Appl Environ Microbiol 51:18–24
Muyzer G, deBruyn AC, Schmedding DJM, Bos P, Westbroek P, Kuenen GJ (1987) A combined immunofluorescene-DNA-fluorescence staining technique for enumeration of Thiobacillus ferrooxidans in a population of acidophilic bacteria. Appl Environ Microbiol 53:660–664
Oremland RS, Umberger C, Culbertson CW, Smith RL (1984) Denitrification in San Francisco Bay intertidal sediments. Appl Environ Microbiol 47:1106–1112
Paerl HW, Bebout BM, Prufert LE (1989) Naturally occurring patterns of oxygenic photosynthesis and nitrogen fixation in marine microbial mats: Physiological and ecological ramifications. In: Cohen Y, Rosenberg E (eds) Microbial Mats: Physiological Ecology of Benthic Microbial Communities. Amer Soc Microbiol, Washington, DC, pp 326–341
Pfaender FK, Bartholomew GW (1982) Measurement of aquatic biodegradation rates by determining heterotrophic uptake of radiolabeled pollutants. Appl Environ Microbiol 44:159–164
Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948
Revsbech NP, Ward DM (1984) Microprofiles of dissolved substances and photosynthesis in microbial mats measured with microelectrodes. In: Cohen Y, Castenholz R, Halvorson H (eds) Microbial Mats: Stromatolites. Alan R Liss New York, pp 171–188
Satsangee R, Ghosh P (1990) Anaerobic degradation of phenol using an acclimated mixed culture. Appl Microbiol Biotechnol 34:127–130
Shea TB (1994) An inexpensive densitometric analysis system using a Macintosh computer and a desktop scanner. Biotechniques 16:1126–1128
Shiaris MP (1989a) Phenanthrene mineralization along a natural salinity gradient in an urban estuary, Boston Harbor, Massachusetts. Microb Ecol 18:135–146
Shiaris MP (1989b) Seasonal biotransformation of naphthalene, phenanthrene, and benzo[a]pyrene in surficial estuarine sediments. Appl Environ Microbiol 55:1391–1399
Smith SV, Hollibaugh JT, Dollar SJ, Vink S (1989) Tomales Bay, California: A case for carbon controlled nitrogen cycling. Limnol Oceanogr 34:37–52
Smith MR (1990) The biodegradation of aromatic hydrocarbons by bacteria. Biodegrad 1:191–206
Song B, Haggblom MM, Zhou J, Tiedje JM, Palleroni NJ (1999) Taxonomic characterization of denitrifying bacteria that degrade aromatic compounds and description of Azoarcus toluvorans sp. nov. and Azoarcus toluclasticus sp. nov. Int J Syst Bacteriol 49:1129–1140
Sorensen J (1978) Denitrification rates in a marine sediment as measured by the acetylene inhibition technique. Appl Environ Microbiol 36:139–143
Spain JC, Pritchard PH, Bourquin AW (1980) Effects of adaptation on biodegradation rates in sediment/water cores from estuarine and freshwater environments. Appl Environ Microbiol 40:726–734
Stucki G, Alexander M (1987) Role of dissolution rate and solubility in biodegradation of aromatic compounds. Appl Environ Microbiol 53:292–297
Systat: Statistics, Version 5.2 Edition. 1992. Systat, Inc, Evanston, IL, 724 pp.
Ward BB, Cockcroft AR (1993) Immunofluorescence detection of the denitrifying strain Pseudomonas stutzeri (ATCC 14405) in seawater and intertidal sediment environments. Microb Ecol 25:233–246
Ward BB, Cockcroft AR, Kilpatrick KA (1993) Antibody and DNA probes for detection of nitrite reductase in seawater. J Gen Microbiol 139:2285–2293
Ward BB, Priscu JC (1997) Detection and characterization of denitrifying bacteria in an ice-covered Antarctic Lake. Hydrobiologia 347:57–68
Ward DM, Brock TD (1978) Hydrocarbon biodegradation in hypersaline environments. Appl Environ Microbiol 35:353–359
Yoshinari T, Knowles R (1976) Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochem Biophys Commun 69:705–710
Zeyer J, Kuhn EP, Schwarzenbach RP (1986) Rapid microbial mineralization of toluene and 1,3-dimethylbenzene in the absence of molecular oxygen. Appl Environ Microbiol 52:944–947
Zumif WC (1992) The denitrifying prokaryotes. In: Ballows A (ed) The Prokaryotes, 2nd ed. Springer-Verlag, New York, pp 554–582
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Golet, D.S., Ward, B.B. Vertical distribution of denitrification potential, denitrifying bacteria, and benzoate utilization in intertidal microbial mat communities. Microb Ecol 42, 22–34 (2001). https://doi.org/10.1007/s002489900184
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s002489900184