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Applied and Environmental Microbiology, March 2004, p. 1593-1599, Vol. 70, No. 3
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.3.1593-1599.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Impact of Violacein-Producing Bacteria on Survival and Feeding of Bacterivorous Nanoflagellates

Carsten Matz,^1,2,* Peter Deines,^1, Jens Boenigk,³ Hartmut Arndt,³ Leo Eberl,⁴ Staffan Kjelleberg,² and Klaus Jürgens^1,5

Department of Physiological Ecology, Max Planck Institute for Limnology, D-24302 Plön,¹ Department of General Ecology and Limnology, Zoological Institute, University of Cologne, D-50923 Cologne,³ Baltic Sea Research Institute Warnemünde, D-18119 Rostock, Germany,⁵ School of Biotechnology and Biomolecular Sciences, Centre for Marine Biofouling and Bio-Innovation, University of New South Wales, Sydney 2052, New South Wales, Australia,² Department of Microbiology, Institute of Plant Biology, University of Zürich, CH-8008 Zürich, Switzerland⁴

Received 8 September 2003/ Accepted 1 December 2003

We studied the role of bacterial secondary metabolites in the context of grazing protection against protozoans. A model system was used to examine the impact of violacein-producing bacteria on feeding rates, growth, and survival of three common bacterivorous nanoflagellates. Freshwater isolates of Janthinobacterium lividum and Chromobacterium violaceum produced the purple pigment violacein and exhibited acute toxicity to the nanoflagellates tested. High-resolution video microscopy revealed that these bacteria were ingested by the flagellates at high rates. The uptake of less than three bacteria resulted in rapid flagellate cell death after about 20 min and cell lysis within 1 to 2 h. In selectivity experiments with nontoxic Pseudomonas putida MM1, flagellates did not discriminate against pigmented strains. Purified violacein from cell extracts of C. violaceum showed high toxicity to nanoflagellates. In addition, antiprotozoal activity was found to positively correlate with the violacein content of the bacterial strains. Pigment synthesis in C. violaceum is regulated by an N-acylhomoserine lactone (AHL)-dependent quorum-sensing system. An AHL-deficient, nonpigmented mutant provided high flagellate growth rates, while the addition of the natural C. violaceum AHL could restore toxicity. Moreover, it was shown that the presence of violacein-producing bacteria in an otherwise nontoxic bacterial diet considerably inhibited flagellate population growth. Our results suggest that violacein-producing bacteria possess a highly effective survival mechanism which may exemplify the potential of some bacterial secondary metabolites to undermine protozoan grazing pressure and population dynamics.

C. M. and P. D. contributed equally to this work.

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