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Feeding Characteristics of an Amoeba (Lobosea: Naegleria) Grazing Upon Cyanobacteria: Food Selection, Ingestion and Digestion Progress

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Abstract

Bacterivory by heterotrophic nanoflagellates and ciliates has been widely studied in aquatic environments, but data on the grazing of amoebae, are still scarce. From the water samples of Dianchi Lake (Kunming, Yunnan Province, China), we isolated an amoeba, designated as Naegleria sp. strain W2, which had potent grazing effects on some kind of cyanobacteria. The food selection mechanism and the digestion process of the amoeba were investigated in batch experiments. Predation experiments showed that filamentous cyanobacteria (e.g., Anabaena, Cylindrospermum, Gloeotrichia, and Phormidium) were readily consumed, with clearance rates ranging from 0.332 to 0.513 nL amoeba−1 h−1. The tight threads (Oscilltoria) and aggregates (Aphanizomenon) could not be ingested; however, their sonicated fragments were observed inside food vacuoles, suggesting that their morphologies prevent them from being ingested. Live video microscopy noted that unicellular Chroococcaceae (e.g., Synechococcus, Aphanocapsa, and Microcystis) were excreted after ingestion, indicating that food selection takes place inside food vacuoles. To determine whether the tastes or the toxins prevented them from being digested, heat-killed cells were retested for predation. Digestion rates and ingestion rates of the amoebae for filamentous cyanobacteria were estimated from food vacuole content volume. Through a “cold-chase” method, we found that the food vacuole contents declined exponentially in diluted amoebae cells, and digestion rates were relatively constant, averaging about 1.5% food vacuole content min−1 at 28°C. Ingestion strongly depended on the satiation status of the amoebae, starved amoebae fed at higher rates compared with satiated amoebae. Our results suggest that the food selection and food processing mechanisms of the amoeba are similar to those of interception feeding flagellates; however, filamentous cyanobacteria cannot obtain a refuge under the grazing pressure of phagotrophic amoebae, which may widen our knowledge on the grazing of protists.

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References

  1. Allen, MM (1968) Simple conditions for growth of unicellular blue-green on plates. J Phycol 4: 1–4

    Article  CAS  Google Scholar 

  2. Boenigk, J, Arndt, H (2000) Particle handling during interception feeding by four species of heterotrophic nanoflagellates. J Eukaryot Microbiol 47: 350–358

    Article  PubMed  CAS  Google Scholar 

  3. Boenigk, J, Arndt, H (2000) Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choannoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhynchomonas nasuta. Aquat Microb Ecol 22: 243–249

    Article  Google Scholar 

  4. Boenigk, J, Matz, AC, Jurgens, K, Arndt, H (2001) Confusing selective feeding with differential digestion in bacterivorous nanoflagellates. J Eukaryot Microbiol 48: 425–432

    Article  PubMed  CAS  Google Scholar 

  5. Boenigk, J, Matz, C, Jurgens, K, Arndt, H (2001) The influence of preculture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb Ecol 42: 168–176

    PubMed  Google Scholar 

  6. Boenigk, J, Arndt, H (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie Van Leeuwenhoek 81: 465–480

    Article  PubMed  Google Scholar 

  7. Burkholder, JM, Glasgow Jr, HB (1997) Trophic controls on stage transformations of a toxic ambush-predator dinoflagellate. J Eukaryot Microbiol 44: 200–205

    Article  PubMed  CAS  Google Scholar 

  8. Cater, RF (1970) Description of a Naegleria sp. Isolated from two cases of primary amoebic meningo-encephalitis, and of the experimental pathological changes induced by it. J Pathol 100: 217–244

    Article  PubMed  Google Scholar 

  9. Christaki, U, Courties, C, Karayanni, H, Giannakourou, A, Maravelias, C, Kormas, KA, Lebaron, P (2002) Dynamic characteristics of Prochlorococcus and Synechococcus consumption by bacterivorous nanoflagellates. Microb Ecol 43: 341–352

    Article  PubMed  CAS  Google Scholar 

  10. Chrzanowski, TH, Simek, K (1990) Prey-size selection by freshwater flagellated protozoa. Limnol Oceanogr 35: 1429–1436

    Google Scholar 

  11. Dolan, JR, Coats, DW (1991) Preliminary prey digestion in a predacious estuarine ciliate and the use of digestion data to estimate ingestion. Limnol Oceanogr 36: 558–565

    Article  Google Scholar 

  12. Dolan, JR, Simek, K (1997) Processing of ingested matter in Strombidium sulcatum, a marine ciliate (oligotrichida). Limnol Oceanogr 42: 393–397

    Google Scholar 

  13. Dolan, JR, Simek, K (1998) Ingestion and digestion of an autotrophic picoplankter, Synchococcus, by a heterotrophic nanoflagellate, Bodo saltans. Limnol Oceanogr 43: 1740–1746

    Google Scholar 

  14. Farmer, JN (1980) The Protozoa: Introduction to Protozoology. Mosby. St. Louis, MO

    Google Scholar 

  15. Gonzalez, JM, Iirberri, J, Egea, L, Barcina, I (1990) Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl Environ Microbiol 56: 1851–1857

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  17. Hahn, MW, Moore, ER, Hofle, MG (1999) Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl Environ Microbiol 65: 25–35

    PubMed  CAS  Google Scholar 

  18. Hahn, MW, Moore, ER, Hofle, MG (2000) Role of microcolony formation in the protistan grazing defense of the aquatic bacterium Pseudomonas sp. Mwh1. Microb Ecol 39: 175–185

    PubMed  Google Scholar 

  19. Hahn, MW, Hofle, MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35: 113–121

    Article  PubMed  CAS  Google Scholar 

  20. Heinbokel, JF (1978) Studies on the functional role of tintinnids in the Southern California bight. I. Grazing and growth rates in laboratory cultures. Mar Biol 47: 117–189

    Google Scholar 

  21. Jungmann, D (1992) Toxic compounds isolated from Microcystis aeruginosa PCC 7806 that are more active to Daphnia than two microcystins. Limnol Oceanogr 37: 1777–1793

    Article  CAS  Google Scholar 

  22. Jurgens, K, Matz, C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81: 413–434

    Article  PubMed  CAS  Google Scholar 

  23. Laybourn-Parry, J, Jones, K, Holdich, JP (1987) Grazing by Mayorella sp. (protozoa: Sarcodina) on cyanobacteria. Funct Ecol 1: 99–104

    Article  Google Scholar 

  24. Lorenzen, M, Batley, G (1988) Chemical speciation and trace element toxicity. Chem Aust 55: 363–366

    Google Scholar 

  25. Marshall, MM, Naumovitz, D, Ortega, Y, Sterling, CR (1997) Waterborne protozoan pathogens. Clin Microbiol Rev 10: 67–85

    PubMed  CAS  Google Scholar 

  26. Matz, C, Jurgens, K (2001) Effects of hydrophobic and electrostatic cell surface properties of bacteria on feeding rates of heterotrophic nanoflagellates. Appl Environ Microbiol 67: 814–820

    Article  PubMed  CAS  Google Scholar 

  27. Matz, C, Boenigk, J, Arndt, H, Jurgens, K (2002) Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat Microb Ecol 27: 137–148

    Article  Google Scholar 

  28. Matz, C, Jurgens, K (2003) Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb Ecol 45: 384–398

    Article  PubMed  CAS  Google Scholar 

  29. Matz, C, Deines, P, Boenigk, J, Arndt, H, Eberl, L, Kjelleberg, S, Jurgens, K (2004) Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl Environ Microbiol 70: 1593–1599

    Article  PubMed  CAS  Google Scholar 

  30. Matz, C, Jurgens, K (2005) High motility reduces grazing mortality of planktonic bacteria. Appl Environ Microbiol 71: 921–929

    Article  PubMed  CAS  Google Scholar 

  31. Pfandl, K, Posch, T, Boenigk, J (2004) Unexpected effects of prey dimensions and morphologies on the size selective feeding by two bacterivorous flagellates (Ochromonas sp. and Spumella sp.). J Eukaryot Microbiol 51: 626–633

    Article  PubMed  Google Scholar 

  32. Posch, T, Jezbera, J, Vrba, J, Simek, K, Pernthaler, J, Andreatta, S, Sonntag, B (2001) Size selective feeding in Cyclidium glaucoma (ciliophora, scuticociliatida) and its effects on bacterial community structure: a study from a continuous cultivation system. Microb Ecol 42: 217–227

    Article  PubMed  Google Scholar 

  33. Rohrlack, T, Dittmann, E, Henning, M, Borner, T, Kohl, JG (1999) Role of microcystins in poisoning and food ingestion inhibition of Daphnia galeata caused by the cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 65: 737–739

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  35. Sigee, DC, Glenn, R, Andrews, EG, Bellinger, RD, Butler, HAS, Hendry, RD (1999) Biological control of cyanobacteria: principles and possibilities. Hydrobiolgia 395–396: 161–172

    Article  Google Scholar 

  36. Simek, K, Vrba, J, Pernthaler, J, Posch, T, Hartman, P, Nedoma, J, Psenner, R (1997) Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl Environ Microbiol 36: 587–595

    Google Scholar 

  37. Simek, K, Nedoma, J, Pernthaler, J, Posch, T, Dolan, JR (2002) Altering the balance between bacterial production and protistan bacterivory triggers shifts in freshwater bacterial community composition. Antonie Van Leeuwenhoek 81: 453–463

    Article  PubMed  CAS  Google Scholar 

  38. Suzuki, MT, Rappě, MS (1997) Bacterial diversity among small-subunit rRNA gene clones and cellular isolates from the same seawater sample. Appl Environ Microbiol 63: 983–989

    PubMed  CAS  Google Scholar 

  39. Wiesse, T (1993) Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. Adv Microb Ecol 13: 327–369

    Google Scholar 

  40. Wright, SJ, Redhead, K, Maudsley, H (1981) Acanthamoeba castellanii, a predator of cyanobacteria. J Gen Microbiol 125: 293–300

    Google Scholar 

  41. Wu, QL, Boenigk, J, Hahn, MW (2004) Successful predation of filamentous bacteria by a nanoflagellate challenges current models of flagellate bacterivory. Appl Environ Microbiol 70: 332–339

    Article  PubMed  CAS  Google Scholar 

  42. Yamamoto, Y (1981) Observations on the occurrence of microbial agents which cause lysis of blue-green algae in lake Kasumigaura. Jpn J Limnol 42: 20–27

    Google Scholar 

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Authors and Affiliations

  1. National Laboratory of Protein Engineering and Plant Genetic Engineering, College of Life Sciences, Peking University, Beijing, 100871, China

    Liu Xinyao, Shi Miao, Gao Yin & An Chencai

  2. College of Chemistry and Environment Engineering, Beijing Technology and Business University, Beijing, 100037, China

    Liao Yonghong

  3. Key Laboratory of Yunnan Agriculture Biotechnology, Kunming, 650223, Yunnan Province, China

    Zhang Zhongkai

  4. College of Environmental Sciences, Peking University, Beijing, 100871, China

    Wen Donghui & Wu Weizhong

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  1. Liu Xinyao
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  2. Shi Miao
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  3. Liao Yonghong
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Correspondence to An Chencai.

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Xinyao, L., Miao, S., Yonghong, L. et al. Feeding Characteristics of an Amoeba (Lobosea: Naegleria) Grazing Upon Cyanobacteria: Food Selection, Ingestion and Digestion Progress. Microb Ecol 51, 315–325 (2006). https://doi.org/10.1007/s00248-006-9031-2

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  • DOI: https://doi.org/10.1007/s00248-006-9031-2

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