Ectoenzyme kinetics in Florida Bay: Implications for bacterial carbon source and nutrient status Article DOI:
Cite this article as: Williams, C.J. & Jochem, F.J. Hydrobiologia (2006) 569: 113. doi:10.1007/s10750-006-0126-z Abstract
Ectoenzyme kinetics [alkaline phosphatase, aminopeptidase (AM), lipase, α-glucosidase, and β-glucosidase] were determined over a seasonal cycle at four stations, Little Madeira Bay (northeast), Duck Key (east), Bob Allen Key (south-central), and Whipray Basin (north-central), which represent distinct regions of Florida Bay. Spatial and temporal variations in ectoenzyme kinetics were related to biotic and abiotic drivers in order to discern potential ectoenzyme substrate sources. Generally, ectoenzyme activities were higher in the central bay and lowest in the eastern bay. One pronounced exception was AM activity, which was highest at the mangrove fringe along the northeastern bay and reflected increased contribution of organic nitrogen inputs from upstream Everglades wetlands. When ectoenzymes were normalized to bacterial abundances, these trends dissipated and highest cell-specific activities were observed consistently in the south-central region. Relationships between ectoenzyme kinetics and environmental and biological parameters were complex, but three main spatially determined differences were discernable. Ectoenzyme kinetics were controlled by phosphorus availability in the eastern bay, by organic matter availability in the south-central bay, by microbial community composition and organic matter availability in northeastern bay (wetlands transition area), and by microbial community composition in the north-central bay. These differences in enzyme kinetics further support the hypothesis of distinct microbial communities in different regions of Florida Bay and provide insight into biogeochemical cycles and the microbial food web within Florida Bay.
Keywords alkaline phosphatase aminopeptidase microbial food web estuary Florida Everglades References Arnosti, C., Durkin, S., Jeffrey, W. H. 2005 Patterns of extracellular activities among pelagic marine microbial communities: implications for cycling of dissolved organic carbon Aquatic Microbial Ecology 38 135 145 Google Scholar Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., Thingstad, F. 1983 The ecological role of water-column microbes in the sea Marine Ecology Progress Series 10 257 263 Google Scholar Azam, F. 1989 Microbial control of oceanic carbon flux: the plot thickens Science 280 694 696 CrossRef Google Scholar Boyer, J. N., Fourqurean, J. W., Jones, R. D. 1997 Spatial characterization of water quality in Florida Bay and Whitewater Bay by multivariate analyses: zones of similar influence Estuaries 20 743 758 CrossRef Google Scholar Boyer, J. N., Fourqurean, J. W., Jones, R. D. 1999 Seasonal and long-term trends in the water quality of Florida Bay (1989–1997) Estuaries 22 417 430 CrossRef Google Scholar Chróst, R. J. 1989 Characterization and significance of beta-glucosidase activity in lake water Limnology and Oceanography 34 660 672 Google Scholar Chróst, R. J., Overbeck, J. 1987 Kinetics of alkaline phosphatase activity and phosphorus availability for phytoplankton and bacterioplankton in Lake Plußsee (north German eutrophic lake) Microbial Ecology 13 229 248 CrossRef Google Scholar Cotner, J. B., Sada, R. H., Bootsma, H., Johengen, T., Cavaletto, J. F., Gardner, W. S. 2000 Nutrient limitation of heterotrophic bacteria in Florida Bay Estuaries 23 611 620 CrossRef Google Scholar Cunha, M. A., Almeida, M. A., Alcântara, F. 2000 Patterns of ectoenzymatic and heterotrophic bacterial activities along a salinity gradient in a shallow tidal estuary Marine Ecology Progress Series 204 1 12 Google Scholar Cunha, M. A., Almeida, M. A., Alcântara, F. 2001 Short-term responses of the natural planktonic bacterial community to the changing water properties in an estuarine environment: ectoenzymatic activity, glucose incorporation, and biomass production Microbial Ecology 42 69 79 PubMed Google Scholar Fourqurean, J. W., Jones, R. D., Zieman, J. C. 1993 Processes influencing water column nutrient characteristics and phosphorus limitation of phytoplankton biomass in Florida Bay, FL, USA: inferences from spatial distributions Estuarine, Coastal and Shelf Science 36 295 314 CrossRef Google Scholar Glibert, P. M., Neil, C. A., Hollander, D., Revilla, M., Hoare, A., Alexander, J., Murasko, S. 2004 Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay Marine Ecology Progress Series 280 73 83 Google Scholar Healey, F. P., Hendzel, L. L. 1979 Fluorometric measurements of alkaline phosphatase activity in algae Freshwater Biology 9 429 439 CrossRef Google Scholar Hoppe, H.-G. 1993 Use of fluorogenic midel substrates for extracellular enzyme activity (EEA) measurement of bacteria Kemp, P. F. Sherr, B. F. Sherr, E. B. Cole, J. J. eds. Handbook of methods in aquatic microbial ecology Lewis Publishers Boca Raton 423 430 Google Scholar Hoppe, H.-G., Arnosti, C., Herndl, G. F. 2002 Ecological significance of bacterial enzyme in the marine environment Burns, R. G. Dick, R. P. eds. Enzyme in the environment: activity, ecology, and applications Marcel Dekker, Inc New York 73 107 Google Scholar Hoppe, H.-G. 2003 Phosphatase activity in the sea Hydrobiologia 493 187 200 CrossRef Google Scholar Jochem, F. J. 2001 Morphology and DNA content of bacterioplankton in the northern Gulf of Mexico: analysis by epifluorescence microscopy and flow cytometry Aquatic Microbial Ecology 25 179 194 Google Scholar Karner, M., Ferrier-Pagès, C., Rassoulzadegan, F. 1994 Phagotrophic nanoflagellates contribute to occurrence of alpha-glucosidase and aminopeptidase in marine environments Marine Ecology Progress Series 114 237 244 Google Scholar Kelble, C. R., Ortner, P. B., Hitchcock, G. L., Boyer, J. N. 2005 Attenuation of photosynthetically available radiation (PAR) in Florida Bay: potential for light limitation of primary production Estuaries 28 560 571 CrossRef Google Scholar Lavrentyev, P. J., Bootsma, H. A., Johengen, T. H., Cavaletto, J. F., Gardner, W. S. 1998 Microbial plankton response to resource limitation: insight from the community structure and seston stoichiometry in Florida Bay, USA Marine Ecology Progress Series 165 45 57 Google Scholar Maie, N., Yang, C., Miyoshi, T., Parish, K., Jaffé, R. 2005 Chemical characteristics of dissolved organic matter in an oligotrophic subtropical wetland/estuarine ecosystem Limnology and Oceanography 50 23 35 CrossRef Google Scholar Marie, D., Partensky, F., Jacquet, S., Vaulot, D. 1997 Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green 1 Applied and Environmental Microbiology 63 186 193 PubMed Google Scholar Martinez, J., Smith, D. C., Steward, G. F., Azam, F. 1996 Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea Aquatic Microbial Ecology 10 223 230 Google Scholar Martinez, J., Azam, F. 1993 Periplasmic aminopeptidase and alkaline phosphatase in a marine bacterium: implications for substrate processing in the sea Marine Ecology Progress Series 92 89 97 Google Scholar Mead, R., Xu, Y., Chong, J., Jaffé, R. 2005 Sediment and soil organic matter source assessment as revealed by the molecular distribution and carbon isotopic composition of n-alkanes Organic Geochemistry 36 363 370 CrossRef Google Scholar Mohapatra, B. R., Fukami, K. 2004 Production of aminopeptidase by marine heterotrophic nanoflagellates Aquatic Microbial Ecology 34 129 137 Google Scholar Mulholland, M. R., Gobler, C. J., Lee, C. 2002 Peptide hydrolysis, amino acid oxidation, and nitrogen uptake in communities seasonally dominated by Aureococcus anophagefferens Limnology and Oceanography 47 1094 1108 CrossRef Google Scholar Mulholland, M. R., Lee, C., Glibert, P. M. 2003 Extracellular enzyme activity and uptake of carbon and nitrogen along an estuarine salinity and nutrient gradient Marine Ecology Progress Series 258 3 17 Google Scholar Murrell, M. C. 2003 Bacterioplankton dynamics in a subtropical estuary: evidence for substrate limitation Aquatic Microbial Ecology 32 239 250 Google Scholar Nausch, M., Kerstan, E. 2003 The relationship between dissolved carbohydrates and carbohydrate-degrading enzymes in the salinity gradient of the Pomeranian Bight (southern Baltic) Oceanologia 45 437 452 Google Scholar Nausch, M., Nausch, G. 2000 Stimulation of peptidase activity in nutrient gradients in the Baltic Sea Soil Biology & Biochemistry 32 1973 1983 CrossRef Google Scholar Nausch, M., Nausch, G. 2004 Bacterial utilization of phosphorus pools after nitrogen and carbon amendment and its relation to alkaline phosphatase activity Aquatic Microbial Ecology 37 237 245 Google Scholar Phlips, E. J., Lynch, T. C., Badylak, S. 1995 Chlorophyll a, tripton, color, and light availability in a shallow tropical inner-shelf lagoon, Florida Bay, USA Marine Ecology Progress Series 127 223 234 Google Scholar Phlips, E. J., Badylak, S., Lynch, T. C. 1999 Blooms of picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon Limnology and Oceanography 44 1166 1175 CrossRef Google Scholar Phlips, E. J., Badylak, S. 1996 Spatial variability in phytoplankton standing crop and composition in a shallow inner-shelf lagoon, Florida Bay, Florida Bulletin of Marine Science 58 203 216 Google Scholar Rath, J., Schiller, C., Herndl, G. J. 1993 Ectoenzymatic activity and bacterial dynamics along a trophic gradient in the Caribbean Sea Marine Ecology Progress Series 102 89 96 Google Scholar Rudnick, D. T., Chen, Z., Childers, D. L., Boyer, J. N., Fontaine, T. D. 1999 Phosphorus and nitrogen inputs to Florida Bay: the importance of the Everglades watershed Estuaries 22 398 416 CrossRef Google Scholar Sala, M. M., Karner, M., Arin, L., Marrasé, C. 2001 Measurement of ectoenzyme activities as an indication of inorganic nutrient imbalance in microbial communities Aquatic Microbial Ecology 23 301 311 Google Scholar Sala, M. M., Arin, L., Balagué, V., Felipe, J., Guadayol, Ò., Vaqué, D. 2005 Functional diversity of bacterioplankton assemblages in western Antarctic seawaters during late spring Marine Ecology Progress Series 292 13 21 Google Scholar Saliot, A., Cauwet, G., Cahet, G., Mazaudier, D., Daumas, R. 1996 Microbial activities in the Lena River delta and Laptev Sea Marine Chemistry 53 247 254 CrossRef Google Scholar Sebasrián, M., Arístegui, J., Montero, M. A., Niell, F. X. 2004 Kinetics of alkaline phosphatase activity, and effect of phosphate enrichment: a case study in the NW African upwelling region Marine Ecology Progress Series 270 1 13 Google Scholar Sebasrián, M., Niell, F. X. 2004 Alkaline phosphatase activity in marine oligotrophic environments: implications of single-substrate addition assays for potential activity estimations Marine Ecology Progress Series 277 285 290 Google Scholar Solorzano, L., Sharp, J. H. 1980 Determination of total dissolved phosphorus and particulate phosphorus in natural waters Limnology and Oceanography 25 754 758 CrossRef Google Scholar Stoecker, D. K., Gustafson, D. E., Jr. 2003 Cell-surface proteolytic activity of photosynthetic dinoflagellates Aquatic Microbial Ecology 30 175 183 Google Scholar Taylor, G. T., Way, J., Yu, Y., Scranton, M. I. 2003 Ectohydrolase activity in surface waters of the Hudson River and western Long Island Sound estuaries Marine Ecology Progress Series 263 1 15 Google Scholar Unanue, M., Ayo, B., Agis, M., Slezak, D., Herndl, G. J., Iriberri, J. 1999 Ectoenzymatic activity and uptake of monomers in marine bacterioplankton described by a biphasic kinetic model Microbial Ecology 37 36 48 PubMed CrossRef Google Scholar Vrba, J., Callieri, C., Bittl, T., Šimek, K., Bertoni, R., Filandr, P., Hartman, P., Heizlar, J., Macek, M., Nedoma, J. 2004 Are bacteria the major producers of extracellular glycloytic enzymes in aquatic environments International Review of Hydrobiology 89 102 117 CrossRef Google Scholar Weiss, M., Abele, U., Weckesser, J., Welte, W., Schiltz, E., Schulz, G. E. 1991 Molecular architecture and electrostatic properties of a bacterial porin Science 254 1627 1630 PubMed Google Scholar Ziegler, S., Benner, R. 1999 Dissolved organic carbon cycling in a subtropical seagrass-dominated lagoon Marine Ecology Progress Series 180 149 160 Google Scholar Zieman, 1989 Distribution, abundance and productivity of seagrasses and macroalgae in Florida Bay Bulletin of Marine Science 44 292 311 Google Scholar