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Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture

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Abstract

Production of bioluminescence theoretically represents a cost, energetic or otherwise, that could slow Vibrio fischeri growth; however, bioluminescence is also thought to enable full symbiotic colonization of the Euprymna scolopes light organ by V. fischeri. Previous tests of these models have proven inconclusive, partly because they compared nonisogenic strains, or undefined and/or pleiotropic mutants. To test the influence of the bioluminescence-producing lux operon on growth and symbiotic competence, we generated dark ∆luxCDABEG mutants in strains MJ1 and ES114 without disrupting the luxR-luxI regulatory circuit. The MJ1 ∆luxCDABEG mutant out-competed its visibly luminescent parent ~26% per generation in a carbon-limited chemostat. Similarly, induction of luminescence in the otherwise dim ES114 strain slowed growth relative to ΔluxCDABEG mutants. Some culture conditions yielded no detectable effect of luminescence on growth, indicating that luminescence is not always growth limiting; however, luminescence was never found to confer an advantage in culture. In contrast to this conditional disadvantage of lux expression, ES114 achieved ~fourfold higher populations than its ∆luxCDABEG mutant in the light organ of E. scolopes. These results demonstrate that induction of luxCDABEG can slow V. fischeri growth under certain culture conditions and is a positive symbiotic colonization factor.

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Acknowledgments

We thank Melissa Butler, Alecia Septer, Deanna Colton, Anne Dunn, Dawn Adin, and Noreen Lyell for technical assistance, and Karen Visick for sharing strains. Genome information was provided by the Vibrio fischeri Genome Project, at http://ergo.integratedgenomics.com/Genomes/VFI, supported by the W. M. Keck Foundation. This work was supported by a CAREER award to EVS from the National Science Foundation (MCB-0347317), by National Institutes of Health grant R01AI50661, and by a STIR grant from the Army Research Office (49549LSII).

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  1. Department of Microbiology, University of Georgia, 828 Biological Sciences, Athens, GA, 30602, USA

    Jeffrey L. Bose, Charles S. Rosenberg & Eric V. Stabb

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  1. Jeffrey L. Bose
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  2. Charles S. Rosenberg
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  3. Eric V. Stabb
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Correspondence to Eric V. Stabb.

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Communicated by Andreas Brune.

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Bose, J.L., Rosenberg, C.S. & Stabb, E.V. Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture. Arch Microbiol 190, 169–183 (2008). https://doi.org/10.1007/s00203-008-0387-1

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