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Phagotrophy of fluorescently labeled bacteria by an oceanic phytoplankter

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Abstract

Using fluorescently-labeled bacteria and detection by flow cytometry and epifluorescence microscopy, we demonstrate inducible mixotrophy in a marine photosynthetic flagellate, Ochromonas sp. (class Chrysophyceae). Phagotrophic uptake of bacteria increases under conditions of low or limiting light and nutrients, but deceases in periods of prolonged darkness; sustained phagotrophy may require light. In addition, this alga appears to discriminate between and preferentially ingest different types of bacteria. Although this clone is primarily photosynthetic, phagotrophy contributes to its nutrition, especially when light or nutrients limit photosynthesis.

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References

  1. Aaronson S (1974) The biology and ultrastructure of phagotrophy in Ochromonas danica (Chrysophyceae: Chrysomonadida). J Gen Microbiol 83:21–29

    Google Scholar 

  2. Andersson A, Larsson U, Hagstrom A (1986) Size-selective grazing by a microflagellate on pelagic bacteria. Mar Ecol Prog Ser 33:51–57

    Google Scholar 

  3. Andersson A, Falk S, Samuelsson G, Hagstrom A (1989) Nutritional characteristics of a mixotrophic nanoflagellate, Ochromonas sp. Microb Ecol 17:251–262

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  6. Boraas ME, Seale DB, Holen D (1992) Predatory behavior of Ochromonas analyzed with video microscopy. Arch Hydrobiol 123(4):459–468

    Google Scholar 

  7. Caron DA, Sanders RW, Lim EL, Marrase C, Amaral LA, Whitney S, Aoki RB, Porter KG (1993) Light dependent phagotrophy in the freshwater mixotrophic chrysophyte, Dinobryon cylindricium. Microb Ecol 25(1):93–111

    Google Scholar 

  8. Cucci TL, Shumway SE, Brown WS, Newell CR (1989) Using phytoplankton and flow cytometry to analyze grazing by marine organisms. Cytometry 10:659–669

    Google Scholar 

  9. Estep KW, Davis PG, Hargraves PE, Sieburth JMcN (1984) Chloroplast-containing microflagellates in natural populations of North Atlantic nanoplankton, their identification and distribution; including a description of five new species of Chrysochromulina (Prymnesiophyceae). Protistologica 20:613–634

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  12. Gieskes WWC, Kraay GW (1986) Floristic and physiological differences between the shallow and the deep nanophytoplankton community in the euphotic zone of the open tropical Atlantic revealed by HPLC analysis of pigments. Mar Biol 91:567–576

    Google Scholar 

  13. Glover HE, Keller MD, Spinrad RW (1987) The effects of light quality and intensity on photosynthesis and growth of marine eukaryotic and prokaryotic phytoplankton clones. J Exp Mar Biol Ecol 105:137–159

    Google Scholar 

  14. Gonzalez JM, Sherr EB, Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl Environ Micro 56:583–589

    Google Scholar 

  15. Hobbie JE, Daley RJ, Jasper S (1977) Use of Nucleopore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228

    CAS  PubMed  Google Scholar 

  16. Hooks CE, Bidigare RR, Keller MD, Guillard RRL (1988) Coccoid eukaryotic marine ultraplankters with four different HPLC pigment signatures. J Phycol 24:571–580

    Google Scholar 

  17. Ishida Y, Kimura B (1986) Photosynthetic phagotrophy of Chrysophyceae: evolutionary aspects. Microbiol Sci 3:132–135

    Google Scholar 

  18. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638

    Google Scholar 

  19. Marrase C, Lim EL, Caron DA (1992) Seasonal and daily changes in bacterivory in a coastal plankton community. Mar Ecol Prog Ser 82:281–289

    Google Scholar 

  20. Myers J, Graham JR (1956) The role of photosynthesis in the physiology of Ochromonas. J Cell Compar Physiol 47:397–414

    Google Scholar 

  21. Nygaard K, Hessen DO (1990) Use of 14C-protein-labelled bacteria for estimating clearance rates by heterotrophic and mixotrophic flagellates. Mar Ecol Prog Ser 68:7–14

    Google Scholar 

  22. Nygaard K, Tobiesen A (1993) Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38(2):273–279

    Google Scholar 

  23. Ondrusek ME, Bidigare RR, Sweet ST, Defreitas DA, Brooks JM (1991) Distribution of phytoplankton pigments in the North Pacific Ocean in relation to physical and the optical variability. Deep Sea Res 38:243–266

    Google Scholar 

  24. Parke M, Manton I, Clarke B (1955) Studies on marine flagellates. II. Three new species of Chrysochromulina. J Mar Biol Ass UK 34:579–609

    Google Scholar 

  25. Porter KG (1988) Phagotrophic phytoflagellates in microbiol food webs. Hydrobiol 159:89–97

    Google Scholar 

  26. Pringsheim EG (1952) On the nutrition of Ochromonas. Quart J Microscop Sci 93:71–96

    Google Scholar 

  27. Rublee PA, Gallegos CL (1989) Use of fluorescently labelled algae (FLA) to estimate zooplankton grazing. Mar Ecol Prog Ser 51:221–227

    Google Scholar 

  28. Sanders RW, Porter K (1988) Phagotrophic phytoflagellates. In: Marshall KC (ed) Advances in microbiol ecology, vol 10. Plenum Publ Corp, New York, pp 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. 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 

  32. Sieburth JMcN (1988) The nanoalgal peak in the dim oceanic pycnocline: is photosynthesis augmented by microparticulates and their bacterial consortia? In: Agegian CR (ed) Biogeochemical cycling and fluxes between the deep euphotic zone and other oceanic realms. Natl Undersea Res Progr Res Rep 88-1, pp 101–130

  33. Smith RC, Baker KS, Dunstan P (1981) Fluorometric techniques for the measurement of ocean chlorophyll in the support of remote sensing. Ref Rpt Scripps Inst Oceanogr 18-17, pp 1–14

  34. Wood AM, VanValen LM (1990) Paradox lost? On the release of energy-rich compounds by phytoplankton. Mar Microb Food Webs 4:103–116

    Google Scholar 

  35. Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Res 10:443–448

    Google Scholar 

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Authors and Affiliations

  1. Bigelow Laboratory for Ocean Sciences, McKown Point, West Boothbay Harbor, 04575, Maine, USA

    M. D. Keller, E. M. Haugen & T. L. Cucci

  2. Oregon Institute for Marine Biology, University of Oregon, 97420, Charleston, Oregon, USA

    L. P. Shapiro

  3. College of Oceanography, Oregon State University, 97331, Corvallis, Oregon, USA

    E. B. Sherr & B. F. Sherr

Authors
  1. M. D. Keller
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  2. L. P. Shapiro
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  3. E. M. Haugen
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  4. T. L. Cucci
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  5. E. B. Sherr
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  6. B. F. Sherr
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Correspondence to: M.D. Keller

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Keller, M.D., Shapiro, L.P., Haugen, E.M. et al. Phagotrophy of fluorescently labeled bacteria by an oceanic phytoplankter. Microb Ecol 28, 39–52 (1994). https://doi.org/10.1007/BF00170246

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  • DOI: https://doi.org/10.1007/BF00170246

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