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Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobryon cylindricum

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Abstract

The mixotrophic (bacterivorous), freshwater chrysophyte Dinobryon cylindricum was cultured under a variety of light regimes and in bacterized and axenic cultures to investigate the role of phototrophy and phagotrophy for the growth of this alga. D. cylindricum was found to be an obligate phototroph. The alga was unable to survive in continuous darkness even when cultures were supplemented with high concentrations of bacteria, and bacterivory ceased in cultures placed in the dark for a period longer than one day. Axenic growth of the alga was poor even in an optimal light regime. Live bacteria were required for sustained, vigorous growth of the alga in the light. Carbon (C), nitrogen (N), and phosphorus (P) budgets determined for the alga during growth in bacterized cultures indicated that bacterial biomass ingested by the alga may have contributed up to 25% of the organic carbon budget of the alga. Photosynthesis was the source of most (⩾75%) of the organic carbon of the alga. D. cylindricum populations survived but did not grow when cultured in a continuous low light intensity (30 μE m−2 sec−1), or in a light intensity of 150 μE m−2 sec−1 for only two hours each day. Net efficiency of incorporation of bacterial C, N, and P into algal biomass under these two conditions was zero (i.e., no net algal population growth). We conclude that the primary function of bacterivorous behavior in D. cylindricum may be to provide essential growth factor(s) or major nutrients for photosynthetic growth, or to allow for the survival of individuals during periods of very low light intensity or short photoperiod.

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References

  1. Andesson A, Falk S, Samuelsson G, Hagström Å (1989) Nutritional characteristics of a mixotrophic nanoflagellate, Ochromonas sp. Microb Ecol 17:117–128

    Google Scholar 

  2. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Google Scholar 

  3. Beers JR, Reid FMH, Stewart GL (1982) Seasonal abundance of the microplankton population in the North Pacific central gyre. Deep-Sea Res 29:227–245

    Google Scholar 

  4. Bird DF, Kalff J (1986) Bacterial grazing by planktonic lake algae. Science 231:493–495

    Google Scholar 

  5. Bird DF, Kalff J (1987) Algal phagotrophy: Regulating factors and importance relative to photosynthesis in Dinobryon (Chrysophyceae). Limnol Oceanogr 32:277–284

    Google Scholar 

  6. Bird DF, Kalff J (1989) Phagotrophic sustenance of a metalimnetic phytoplankton peak. Limnol Oceanogr 34:155–162

    Google Scholar 

  7. Boraas ME, Estep KW, Johnson PW, Sieburth JM (1988) Phagotrophic phototrophs: The ecological significance of mixotrophy. J Protozool 35:249–252

    Google Scholar 

  8. Bratbak G (1985) Bacterial biovolume and biomass estimations. Appl Environ Microbiol 49:1488–1493

    Google Scholar 

  9. Caron DA, Goldman JC (1990) Protozoan nutrient regeneration. In: Capriulo GM (ed) Ecology of marine protozoa. Oxford University Press, New York, pp 283–306

    Google Scholar 

  10. Caron DA, Lim EL (1990) Phagotrophic nanoplanktonic algae in oceanic environments: High abundances in surface waters of the Sargasso Sea. EOS Trans Am Geophys Un 71:161–162

    Google Scholar 

  11. Caron DA, Porter KG, Sanders RW (1990) Carbon, nitrogen, and phosphorus budgets for the mixotrophic phytoflagellate Poterioochromonas malhamensis (Chyosophyceae) during bacterial ingestion. Limnol Oceanogr 35:433–443

    Google Scholar 

  12. Estep KW, Davis PG, Keller MD, Sieburth JM (1986) How important are oceanic algal nanoflagellates in bacterivory. Limnol Oceanogr 31:646–650

    Google Scholar 

  13. Fenchel T (1982) Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar Ecol Prog Ser 8:225–231

    Google Scholar 

  14. Goldman JC, Caron DA, Andersen OK, Dennett MR (1985) Nutrient cycling in a microflagellate food chain. I. Nitrogen dynamics. Mar Ecol Prog Ser 24:231–242

    Google Scholar 

  15. Goldman JC, Caron DA, Dennett MR (1987) Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C: N ratio. Limnol Oceanogr 32:1239–1252

    Google Scholar 

  16. Haffner GD, Griffith M, Hebert PDN (1984) Phytoplankton community structure and distribution in the nearshore zone of Lake Ontario. Hydrobiologia 114:51–66

    Google Scholar 

  17. Heinbokel JF (1978) Studies of the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar Biol 47:177–189

    Google Scholar 

  18. Hutchinson GE (1967) A treatise of limnology, vol. 2. Introduction to lake biology and limnoplankton. John Wiley & Sons, New York

    Google Scholar 

  19. Keller MD, Shapiro LP, Haugen EM, Cucci TL, Sherr BE, Sherr EB (1988) Phagotrophy by a photosynthetic marine phytoplankten demonstrated by fluorescence-labelled bacteria and flow cytometry. EOS Trans Am Geophys Un 69:1116

    Google Scholar 

  20. Kimura B, Ishida Y (1986) Possible phagotrophic feeding of bacteria in a freshwater red tide Chrysophyceae Uroglena americana. Bull Japan Soc Sci Fish 52:697–701

    Google Scholar 

  21. Kimura B, Ishida Y (1989) Phospholipid as a growth factor of Uroglena americana, a red tide chrysophyceae in Lake Biwa. Nippon Suisan Gakkaishi 55:799–804

    Google Scholar 

  22. Kristiansen J, Andersen RA (1986) Chrysophytes: Aspects and problems. Cambridge University Press, Cambridge

    Google Scholar 

  23. Lehman JT (1976) Ecological and nutritional studies on Dinobryon Ehrenb: Seasonal periodicity and the phosphate toxicity problem. Limnol Oceanogr 21:646–658

    CAS  PubMed  Google Scholar 

  24. Menzel DW, Corwin N (1965) The measurement of total phosphorus in seawater based on the liberation of organically bound fractions by persulfate oxidation. Limnol Oceanogr 10:280–282

    Google Scholar 

  25. Nagata T (1986) Carbon and nitrogen content of natural planktonic bacteria. Appl Environ Microbiol 52:28–32

    Google Scholar 

  26. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford

    Google Scholar 

  27. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Google Scholar 

  28. Sanders RW, Porter KG (1988) Phagotrophic phytoflagellates. Adv Microb Ecol 10:167–192

    Google Scholar 

  29. Sanders RW, Porter KG, Bennett SJ, DeBiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34:673–687

    Google Scholar 

  30. Sanders RW, Porter KG, Caron DA (1990) Relationship between phototrophy and phagotrophy in the mixotrophic chrysophyte Poterioochromonas malhamensis. Microb Ecol 19:97–109

    Google Scholar 

  31. Sandgren CD (1988) The ecology of chrysophyte flagellates: Their growth and perennation strategies as freshwater phytoplankton. In: Sandgren CD (ed) Growth and reproduction strategies of freshwater phytoplankton. Cambridge University Press, Cambridge, pp 9–104

    Google Scholar 

  32. Sherr BF, Sherr EB, Berman T (1983) Grazing, growth, and ammonium excretion rates of a heterotrophic microflagellate fed with four species of bacteria. Appl Environ Microbiol 45:1196–1201

    Google Scholar 

  33. Sherr BF, Sherr EB, Paffenhöfer G-A (1986) Phagotrophic protozoa as food for metazoans: A “missing” trophic link in marine pelagic food webs. Mar Microb Food Webs 1:61–80

    Google Scholar 

  34. Sherr BF, Sherr EB, Fallon RD (1987) Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol 53:958–965

    Google Scholar 

  35. Sherr BF, Sherr EB, Rassoulzadegan F (1988) Rates of digestion of bacteria by marine phagotrophic protozoa: Temperature dependence. Appl Environ Microbiol 54:1091–1095

    Google Scholar 

  36. Sieburth JM (1984) Protozoan bacterivory in pelagic marine waters. In: Hobbic JE, Williams PJ (ed) Heterotrophic activity in the sea. Plenum Press, New York, pp 405–444

    Google Scholar 

  37. Siver PA, Chock JS (1986) Phytoplankton dynamics in a chrysophysean lake. In: Kritiansen J, Andersen RA (ed) Chrysophytes: Aspects and problems. Cambridge University Press, Cambridge, pp 165–183

    Google Scholar 

  38. Strathmann RR (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol Oceanogr 12:411–418

    Google Scholar 

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Authors and Affiliations

  1. Biology Department, Woods Hole Oceanographic Institution, 02543, Woods Hole, Massachusetts, USA

    David A. Caron, Ee Lin Lim & Linda A. Amaral

  2. Division of Environmental Research, Academy of Natural Sciences of Philadelphia, 19103, Philadelphia, Pennsylvania, USA

    Robert W. Sanders & Rika B. Aoki

  3. Institut de Ciències del Mar, Passeig Nacional, s/n, 08003, Barcelona, Spain

    Celia Marrasé

  4. NASA/Ames Research Center, MS 242-4, 94035-1000, Moffett Field, California, USA

    Sheri Whitney

  5. Department of Zoology, University of Georgia, 30602, Athens, Georgia, USA

    Karen G. Porters

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  1. David A. Caron
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  2. Robert W. Sanders
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  4. Celia Marrasé
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Caron, D.A., Sanders, R.W., Lim, E.L. et al. Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobryon cylindricum . Microb Ecol 25, 93–111 (1993). https://doi.org/10.1007/BF00182132

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  • DOI: https://doi.org/10.1007/BF00182132

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