Abstract
To assess bacterioplankton production in the sea, we have developed a procedure for measuring growth based on incorporation of tritiated thymidine into DNA; the accuracy of this procedure was tested under a variety of laboratory and field conditions. By autoradiography, we have found that for all practical purposes our technique is specific for the nonphotosynthetic bacteria and that virtually all of the “active” bacteria (one-third or more of the total countable bacteria) take up thymidine. We also measured (1) the intracellular isotope dilution of thymidine assessed by parallel experiments with labeled phosphorus, and (2) DNA content of natural marine bacteria (0.2 to 0.6 μm size fraction); a conversion factor derived from these data permitted estimation of production from thymidine incorporation results. A very similar conversion factor was independently derived from the empirical relationship between thymidine incorporation and growth of natural bacterioplankton under controlled conditions. Combined results show that this technique, which can be performed rapidly and easily at sea, provides good estimates of production. Data from Southern California Bight waters, which contain oligotrophic as well as moderately eutrophic regions, show that average bacterioplankton doubling times, like those of the phytoplankton, are on the order of a few days, with fastest growth at depths just below those of greatest phytoplankton abundance. Offshore bacterial production is roughly 5 to 25% of the primary production; thus, at a 50% assimilation efficiency, the bacterioplankton would consume 10 to 50% of the total fixed carbon.
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Literature Cited
Cattolico, R. A. and S. P. Gibbs: Rapid filter method for the microfluorometric analysis of DNA. Analyt. Biochem. 69, 572–582 (1975)
Dunn, O. J. and V. A. Clark: Applied statistics analysis of variance and regression, 387 pp. New York: John Wiley & Sons 1974
Eppley, R. W., S. G. Horrigan, J. A. Fuhrman, E. R. Brooks, C. C. Price and K. Sellner: Origins of dissolved organic matter in Southern California coastal waters: experiments on the role of zooplankton. Mar. Ecol. Prog. Ser. 6, 149–159 (1981)
Fuhrman, J. A.: Influence of method on the apparent size distribution of bacterioplankton cells: epifluorescence microscopy compared to scanning electron microscopy. Mar. Ecol. Prog. Ser. 5, 103–106 (1981)
Fuhrman, J. A., J. W. Ammerman and F. Azam: Bacterioplankton in the coastal euphotic zone: distribution, activity, and possible relationships with phytoplankton. Mar. Biol. 60, 201–207 (1980)
Fuhrman, J. A. and F. Azam: Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl. envirl Microbiol. 39, 1085–1095 (1980)
Haas, L. W. and K. L. Webb: Nutritional mode of several nonpigmented microflagellates from the York River Estuary, Virginia. J. exp. mar. Biol. Ecol. 39, 125–134 (1979)
Harold, F. M.: Inorganic polyphosphates in biology: structure, metabolism, and function. Bact. Rev. 30, 772–794 (1966)
Hollibaugh, J. T., J. A. Fuhrman and F. Azam: Radioactively labeling of natural assemblages of bacterioplankton for use in trophic studies. Limnol. Oceanogr. 25, 172–181 (1980)
Holm-Hansen, O., W. H. Sutcliffe and J. Sharp: Measurement of deoxyribonucleic acid in the ocean and its ecological significance. Limnol. Oceanogr. 13, 507–514 (1968)
Johnson, P. W. and J. McN. Sieburth: Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol. Oceanogr. 24, 928–935 (1979)
King, K. R., J. T. Hollibaugh and F. Azam: Predator-prey interactions between the larvacean Oikopleura dioica and bacterioplankton in enclosed water columns. Mar. Biol. 56, 49–57 (1980)
Lindberg, U. and L. Skoog: A method for the determination of dATP and dTTP in picomole amounts. Analyt. Biochem. 34, 152–160 (1970)
Luria, S. E.: Bacterial protoplasm-composition and organization. In: The bacteria, pp 1–34. Ed. by I. C. Gunsalus and R. Y. Stanier. New York: Academic Press, Inc. 1960
Meyer-Reil, L.-A.: Autoradiography and epifluorescence microscopy combined for the determination of number and spectrum of actively metabolizing bacteria in natural waters. Appl. envirl Microbiol. 36, 506–512 (1978)
Moriarty, D. J. W. and P. C. Pollard: DNA synthesis as a measure of bacterial productivity in seagrass sediments. Mar. Ecol. Prog. Ser. 5 151–156 (1981)
Rogers, A. W.: Techniques of autoradiography, 429 pp. Amsterdam: Elsevier/North-Holland Biomedical Press 1979
Shiba, S., A. Terawaki, J. Taguchi and J. Kawamata: Selective inhibition of formation of deoxyribonucleic acid in Escherichia coli by mitomycin C. Nature, Lond. 183, 1056–1057 (1959)
Strickland, J. D. H. and T. R. Parsons: A practical handbook of seawater analysis, 2nd ed. Bull. Fish. Res. Bd Can. 167, 1–310 (1972)
Tabor, P. S., K. Ohwada and R. R. Colwell: Filterable marine bacteria found in the deep sea: distribution, taxonomy, and response to starvation. Microb. Ecol. 7, 67–83 (1981)
Tate, W. M. and R. C., Clelland: Nonparametric and shortcut statistics, 171 pp. Danville, Illinois: Interstate Printers and Publishers, Inc. 1957
Wallace, D. C. and H. J. Morowitz: Genome size and evolution. Chromosoma 40, 121–126 (1973)
Waterbury, J. B., S. W. Watson, R. R. L. Guillard and L. E. Brand: Widespread occurrence of a unicellular, marine plankton cyanobacterium. Nature, Lond. 277, 293–294 (1979)
Watson, J. D.: Molecular biology of the gene, 662 pp. Menlo Park, California: W. A. Benjamin, Inc. 1970
Watson, S. W., T. J. Novitsky, I. C. Quinby and F. W. Valois: Determination of bacterial number and biomass in the marine environment. Appl. envirl Microbiol. 33, 940–946 (1977)
Williams, P. J. LeB.: Heterotrophic utilization of dissolved organic compounds in the sea. I. Size distribution of population and relationship between respiration and incorporation of growth substances. J. mar. biol. Ass. U.K. 50, 859–870 (1970)
Williams, P. J. LeB. and C. S. Yentsch: An examination of photosynthetic production, excretion of photosynthetic products, and heterotrophic utilization of dissolved organic compounds with reference to results from a coastal subtropical sea. Mar. Biol. 35, 31–40 (1976)
Wright, R. T. and N. M. Shah: The trophic role of glycolic acid in coastal seawater. I. Heterotrophic metabolism in seawater and bacterial cultures. Mar. Biol. 33, 175–183 (1975)
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Communicated by N. D. Holland, La Jolla
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Fuhrman, J.A., Azam, F. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: Evaluation and field results. Mar. Biol. 66, 109–120 (1982). https://doi.org/10.1007/BF00397184
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DOI: https://doi.org/10.1007/BF00397184