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Respiration rates in marine heterotrophic bacteria relate to the cytometric characteristics of bacterioplankton communities

Published online by Cambridge University Press:  03 August 2009

Mathilde Schapira ,
Thomas Pollet ,
James G. Mitchell  and
L. Seuront
Mathilde Schapira*
Affiliation:
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia
Thomas Pollet
Affiliation:
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia UMR CARRTEL, Centre Alpin de Recherche sur les Réseaux Trophiques des Ecosystèmes Limniques, Station d'Hydrologie Lacustre, Université de Savoie, 75 Avenue de Corzent, BP 511, 74203 Thonon les Bains Cedex, France
James G. Mitchell
Affiliation:
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia
L. Seuront
Affiliation:
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia South Australian Research and Development Institute, Aquatic Sciences, West Beach, SA 5022, Australia
*
Correspondence should be addressed to: M. Schapira, Southern Ocean Research Group, Department of Entomology and Zoology, Rhodes University, PO Box 94, Grahamstown, 6040, South Africa email: [email protected]
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Abstract

Respiration in marine bacteria (fraction <0.6 µm) was investigated in 5 distinct coastal ecosystems. Respiration rates were estimated from the decrease of dissolved oxygen (O2) concentrations measured with a fibre-optic oxygen sensor (optode) during short-term incubations (5 to 6 hours) in the dark. Sub-populations of heterotrophic bacteria were defined and enumerated by flow cytometric analysis. Respiration rates ranged from 0.04 to 0.14 µmol O2 l−1 h−1 and were not correlated to total bacteria abundances. In contrast, they significantly increased with the relative proportion of HDNA cells (i.e. high deoxyribonucleic acid content) within the bacterioplankton community. These results stress the need to relate bacterial respiration rates to the absolute and relative abundance of the different cytometrically defined sub-populations found in bacterial assemblages, rather than to total cell counts. This result indicates that only a fraction of bacterial cells may contribute to bacterial respiration, which indicates a reconsideration of the relevance of some previous estimates of bulk bacterial respiration and the related biogeochemical fluxes may be required.

Keywords

marine bacteriarespiration ratesflow cytometrybacteria abundancescommunity structure
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 6 , September 2009 , pp. 1161 - 1169
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Biddanda, B.A., Opsahl, S. and Benner, R. (1994) Plankton respiration and carbon flux through bacterioplankton on the Louisiana shelf. Limnology and Oceanography 39, 1259–1275.CrossRefGoogle Scholar
Bouvier, T., del Giorgio, P.A. and Gasol, J.M. (2007) A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environmental Microbiology 9, 2050–2066.CrossRefGoogle ScholarPubMed
Briand, E., Pringault, O., Jacquet, J. and Torréton, J.P. (2004) The use of oxygen microprobes to measure bacterial respiration for determining bacterioplankton growth efficiency. Limnology and Oceanography Methods 2, 406–416.CrossRefGoogle Scholar
Cole, J.J., Findlay, S. and Pace, P.M. (1988) Bacterial production in fresh water and saltwater ecosystems: a cross-system overview. Marine Ecology Progress Series 43, 1–10.CrossRefGoogle Scholar
Cotner, J.B. and Biddanda, B.A. (2002) Small player, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosytems 5, 105–121.CrossRefGoogle Scholar
del Giorgio, P.A., Cole, J.J. and Cimbleris, A. (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385, 148–151.CrossRefGoogle Scholar
del Giorgio, P.A. and Cole, J.J. (1998) Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecology and Systems 29, 503–541.CrossRefGoogle Scholar
del Giorgio, P.A. and Duarte, C.M. (2002) Respiration in the open ocean. Nature 420, 379–384.CrossRefGoogle ScholarPubMed
Ducklow, H.W. and Carlson, C.A. (1992) Oceanic bacterial production. Advances in Microbial Ecology 12, 113–181.CrossRefGoogle Scholar
Edyvane, K.S. (1996) Issues of South Australian marine environment. In Zann, L.P. and Sutton, D. (eds) State of the marine environment report technical annex 3, State and Territory issues. Ocean Rescue 2000 Program, Department of Environment, Sport and Territories, Canberra.Google Scholar
Edyvane, K.S. (1999) Coastal and marine wetlands in Gulf St. Vincent, South Australia: understanding their loss and degradation. Wetland Ecology and Management 7, 83–104.CrossRefGoogle Scholar
Fenchel, T. (2005) Respiration in aquatic protists. In del Giorgio, P.A. and le B Williams, P.J (eds) Respiration in aquatic ecosystems. New York: Oxford University Press, pp. 47–57.CrossRefGoogle Scholar
Fuhrman, J.A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548.CrossRefGoogle ScholarPubMed
Fuller, M.K., Bone, Y., Gostin, V.A. and Von der Borch, C. (1994) Holocene cool-water carbonate and terrigenous sediments from southern Spencer Gulf, South Australia. Australian Journal of Earth Sciences 41, 353–363.CrossRefGoogle Scholar
Gasol, J.M. and del Giorgio, P.A. (2000) Using flow cytometry for counting natural plankton bacteria and understanding the structure of planktonic bacterial community. Scientia Marina 64, 197–224.CrossRefGoogle Scholar
Gasol, J.M., Zweifel, U.L., Peters, F., Fuhrman, J.A. and Hagstrom, A. (1999) Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Applied and Environmental Microbiology 65, 4475–4483.CrossRefGoogle ScholarPubMed
Gattuso, J.P., Peduzzi, S., Pizay, M.D. and Tonolla, M. (2002) Changes in freshwater bacterial community composition during measurements of microbial and community respiration. Journal of Plankton Research 24, 1197–1206.CrossRefGoogle Scholar
González, N., Anadón, R. and Viesca, L. (2003) Carbon flux through the microbial community in a temperate sea during summer: role of bacterial metabolism. Aquatic Microbial Ecology 33, 117–126.CrossRefGoogle Scholar
Harris, P.T. (1994) Comparison of tropical, carbonate and temperate, siliciclastic tidally dominated sedimentary deposits: examples from the Australian continental shelf. Australian Journal of Earth Sciences 41, 241–254.CrossRefGoogle Scholar
Herbland, A., Le Boutellier, A. and Raimbault, P. (1985) Size structure of phytoplankton biomass in the Equatorial Atlantic Ocean. Deep-Sea Research 32, 819–836.CrossRefGoogle Scholar
Jellett, J.F., Li, W.K.W., Dickie, P.M., Boraie, K. and Kepkay, P.E. (1996) Metabolic activities of bacterioplankton communities assessed by flow cytometry and single carbon substrate utilisation. Marine Ecology Progress Series 136, 213–225.CrossRefGoogle Scholar
Kautsky, H. (1939) Quenching of luminescence by oxygen. Transactions of the Faraday Society 35, 216–219.CrossRefGoogle Scholar
Kritzberg, E.S., Cole, J.J., Pace, M.M. and Granéli, W. (2005) Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquatic Microbial Ecology 38, 103–111.CrossRefGoogle Scholar
Lebaron, P., Servais, P., Baudoux, A.C., Bourrain, M., Courties, C. and Parthuisot, N. (2002) Variation of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry. Aquatic Microbial Ecology 28, 131–140.CrossRefGoogle Scholar
Li, W.K.W., Jellett, J.F. and Dickie, P.M. (1995) DNA distributions in planktonic bacteria stained with TOTO or TO-PRO. Limnology and Oceanography 40, 1485–1495.CrossRefGoogle Scholar
Longnecker, K., Sherr, B.F. and Sherr, E.B. (2005) Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem. Applied and Environmental Microbiology 71, 7737–7749.CrossRefGoogle Scholar
Malone, T.C., Ducklow, H.W., Peele, E.R. and Pike, S.E. (1991) Picoplankton carbon flux in Chesapeake Bay. Marine Ecology Progress Series 78, 11–22.CrossRefGoogle Scholar
Marie, D., Partensky, F., Vaulot, D. and Brussaard, C.P.D. (1999) Numeration of phytoplankton, bacteria and viruses in marine samples. In Robingson, J.P., Darzynkiewicz, Z., Dean, P.N., Orfao, A., Rabinovitch, P., Stewart, C.C., Tanke, H.J. and Wheless, L.L. (eds) Current protocols in cytometry. New York: John Wiley & Sons Inc, Supplement 10, Unit 11.11.Google Scholar
Mary, I., Heywood, J.L., Fuchs, B.M., Amann, R., Tarran, G.A., Burkill, P.H. and Zubkov, M.V. (2006) SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquatic Microbial Ecology 45, 107–113.CrossRefGoogle Scholar
Massana, R., Pedrós-Alió, C., Casamayor, E.O. and Gasol, J.M. (2001) Changes in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters. Limnology and Oceanography 46, 1181–1188.CrossRefGoogle Scholar
Pedrós-Alió, C., Calderón, C. and Gasol, J.M. (2000) Comparative analysis shows that bacterivory, not viral lysis, controls the abundance of heterotrophic prokaryotic plankton. FEMS Microbiology Ecology 32, 157–165.CrossRefGoogle Scholar
Pomeroy, L.R., Sheldon, J. and Sheldon, W.M.J. (1994) Changes in bacterial numbers and leucine assimilation during estimations of microbial respiratory rates in seawater by the precision Winkler method. Applied and Environmental Microbiology 60, 328–332.CrossRefGoogle ScholarPubMed
Pomeroy, L.R., Sheldon, J.E., Sheldon, M. and Peters, F. (1995) Limit of growth and respiration in bacterioplankton in the Gulf of Mexico. Marine Ecology Progress Series 117, 259–268.CrossRefGoogle Scholar
Porter-Smith, R., Harris, P.T., Andersen, O.B., Coleman, R., Greenslade, D. and Jenkins, C.J. (2004) Classification of Australian continental shelf based on predicted sediment threshold exceedance from tidal currents and swell waves. Marine Geology, 211, 1–20.CrossRefGoogle Scholar
Pradeep Ram, A.S.S., Nair, S. and Chandramohan, D. (2003) Bacterial growth efficiency in the tropical estuarine and coastal waters of Goa, southwest coast of India. Microbiology and Ecology 45, 88–96.Google Scholar
Robinson, C. and Williams, P.J. le B. (2005) Respiration and its measurement in surface marine waters. In del Giorgio, P.A. and Williams, P.J. le B. (eds) Respiration in aquatic ecosystems. Oxford University Press, New York, pp. 147–180.CrossRefGoogle Scholar
Schwarz, M.P. (2003) Lincoln, South Australia: Sheet SI53-11 International Index. 1:250 000 Geological Series Explanatory Notes (Geological Survey of South Australia). Adelaide: Primary Industries and Resources South Australia.Google Scholar
Servais, P., Agogue, H., Courties, C., Joux, F. and Lebaron, P. (2001) Are the actively respiring cells (CTC+) those responsible for bacterial production in aquatic environments? FEMS Microbiology Ecology 35, 171–179.CrossRefGoogle ScholarPubMed
Servais, P., Casamayor, E.O., Courties, C., Catala, P., Parthuisot, N. and Lebaron, P. (2003) Activity and diversity of bacterial cells with high and low nucleic acid content. Aquatic Microbial Ecology 33, 41–51.CrossRefGoogle Scholar
Smith, E.M. & Kemp, W.M. (2003) Planktonic and bacterial respiration along an estuarine gradient: response to carbon and nutrient enrichment. Aquatic Microbial Ecology 30, 251–261.CrossRefGoogle Scholar
Strickland, J.D.H. and Parsons, T.R. (1972) A practical handbook of seawater analysis. Bulletin of Fisheries Research Board Canada 167, 1–311.Google Scholar
Tuttle, J.H., Jonas, R.B. and Malone, T.C. (1987) Origin, development and significance of Chesapeake Bay anoxia. In Majumdar, S.K., Hall, L.W. and Austin, H.M. (eds) Contaminant problems and management of living Chesapeake Bay resources. Philadelphia: Pennsylvania Academy of Sciences, pp. 442–472.Google Scholar
Warkentin, M., Freese, H.M., Karsten, U. and Schumman, R. (2007) New and fast method to quantify respiration rates of bacterial and plankton communities in freshwater ecosystems by using optical oxygen sensor spots. Applied and Environmental Microbiology 73, 6722–6729.CrossRefGoogle ScholarPubMed
Williams, P.J. le B. (1981) Microbial contribution to overall marine plankton metabolism; direct measurements of respiration. Oceanologica Acta 4, 359–364.Google Scholar
Zar, J.H. (1996) Biostatistical analysis. Upper Saddle River, NJ: Prentice-Hall International Editions.Google Scholar
Zubkov, M.V., Fuchs, B.M., Burkill, P.H. and Amann, R. (2001) Comparison of cellular and biomass specific activities of dominant bacterioplankton groups in stratified waters of the Celtic Sea. Applied and Environmental Microbiology 67, 5210–5218.CrossRefGoogle ScholarPubMed