Dataset Information

Regulation of Bioluminescence in Photobacterium leiognathi Strain KNH6.

ABSTRACT: Bacterial bioluminescence is taxonomically restricted to certain proteobacteria, many of which belong to the Vibrionaceae. In the most well-studied cases, pheromone signaling plays a key role in regulation of light production. However, previous reports have indicated that certain Photobacterium strains do not use this regulatory method for controlling luminescence. In this study, we combined genome sequencing with genetic approaches to characterize the regulation of luminescence in Photobacterium leiognathi strain KNH6, an extremely bright isolate. Using transposon mutagenesis and screening for decreased luminescence, we identified insertions in genes encoding components necessary for the luciferase reaction (lux, lum, and rib operons) as well as in nine other loci. These additional loci encode gene products predicted to be involved in the tricarboxylic acid (TCA) cycle, DNA and RNA metabolism, transcriptional regulation, and the synthesis of cytochrome c, peptidoglycan, and fatty acids. The mutagenesis screen did not identify any mutants with disruptions of predicted pheromone-related loci. Using targeted gene insertional disruptions, we demonstrate that under the growth conditions tested, luminescence levels do not appear to be controlled through canonical pheromone signaling systems in this strain.Despite the long-standing interest in luminous bacteria, outside a few model organisms, little is known about the regulation and function of luminescence. Light-producing marine bacteria are widely distributed and have diverse lifestyles, suggesting that the control and significance of luminescence may be similarly diverse. In this study, we apply genetic tools to the study of regulation of light production in the extremely bright isolate Photobacterium leiognathi KNH6. Our results suggest an unusual lack of canonical pheromone-mediated control of luminescence and contribute to a better understanding of alternative strategies for regulation of a key bacterial behavior. These experiments lay the groundwork for further study of the regulation and role of bioluminescence in P. leiognathi.

SUBMITTER: Dunn AK

PROVIDER: S-EPMC4626902 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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Regulation of Bioluminescence in Photobacterium leiognathi Strain KNH6.

Dunn Anne K AK Rader Bethany A BA Stabb Eric V EV Mandel Mark J MJ

Journal of bacteriology 20150908 23

<h4>Unlabelled</h4>Bacterial bioluminescence is taxonomically restricted to certain proteobacteria, many of which belong to the Vibrionaceae. In the most well-studied cases, pheromone signaling plays a key role in regulation of light production. However, previous reports have indicated that certain Photobacterium strains do not use this regulatory method for controlling luminescence. In this study, we combined genome sequencing with genetic approaches to characterize the regulation of luminescen ...[more]

PMID: 26350139

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Project description:Sequence analysis of the bacterial luminescence (lux) genes has proven effective in helping resolve evolutionary relationships among luminous bacteria. Phylogenetic analysis using lux genes, however, is based on the assumptions that the lux genes are present as single copies on the bacterial chromosome and are vertically inherited. We report here that certain strains of Photobacterium leiognathi carry multiple phylogenetically distinct copies of the entire operon that codes for luminescence and riboflavin synthesis genes, luxCDABEG-ribEBHA. Merodiploid lux-rib strains of P. leiognathi were detected during sequence analysis of luxA. To define the gene content, organization, and sequence of each lux-rib operon, we constructed a fosmid library of genomic DNA from a representative merodiploid strain, lnuch.13.1. Sequence analysis of fosmid clones and genomic analysis of lnuch.13.1 defined two complete, physically separate, and apparently functional operons, designated lux-rib1 and lux-rib2. P. leiognathi strains lelon.2.1 and lnuch.21.1 were also found to carry lux-rib1 and lux-rib2, whereas ATCC 25521T apparently carries only lux-rib1. In lnuch.13.1, lelon.2.1, lnuch.21.1, and ATCC 25521T, lux-rib1 is flanked upstream by lumQ and putA and downstream by a gene for a hypothetical multidrug efflux pump. In contrast, transposase genes flank lux-rib2 of lnuch.13.1, and the chromosomal location of lux-rib2 apparently differs in lnuch.13.1, lelon.2.1, and lnuch.21.1. Phylogenetic analysis demonstrated that lux-rib1 and lux-rib2 are more closely related to each other than either one is to the lux and rib genes of other bacterial species, which rules out interspecies lateral gene transfer as the origin of lux-rib2 in P. leiognathi; lux-rib2 apparently arose within a previously unsampled or extinct P. leiognathi lineage. Analysis of 170 additional strains of P. leiognathi, for a total of 174 strains examined from coastal waters of Japan, Taiwan, the Philippine Islands, and Thailand, identified 106 strains that carry only a single lux-rib operon and 68 that carry multiple lux-rib operons. Strains bearing a single lux-rib operon were obtained throughout the geographic sampling range, whereas lux-rib merodiploid strains were found only in coastal waters of central Honshu. This is the first report of merodiploidy of lux or rib genes in a luminous bacterium and the first indication that a natural merodiploid state in bacteria can correlate with geography.

Project description:Bacterial-bioluminescence regulation is often associated with quorum sensing. Indeed, many studies have been made on this subject and indicate that the expression of the light-emission-involved genes is density dependent. However, most of these studies have concerned two model species, Aliivibrio fischeri and Vibrio campbellii. Very few works have been done on bioluminescence regulation for the other bacterial genera. Yet, according to the large variety of habitats of luminous marine bacteria, it would not be surprising to find different light-regulation systems. In this study, we used Photobacterium phosphoreum ANT-2200, a piezophilic bioluminescent strain isolated from Mediterranean deep-sea waters (2200-m depth). To answer the question of whether or not the bioluminescence of P. phosphoreum ANT-2200 is under quorum-sensing control, we focused on the correlation between growth and light emission through physiological, genomic and, transcriptomic approaches. Unlike A. fischeri and V. campbellii, the light of P. phosphoreum ANT-2200 immediately increases from its initial level. Interestingly, the emitted light increases at much higher rate at the low cell density than it does for higher cell-density values. The expression level of the light-emission-involved genes stays constant all along the exponential growth phase. We also showed that, even when more light is produced, when the strain is cultivated at high hydrostatic pressure, no change in the transcription level of these genes can be detected. Through different experiments and approaches, our results clearly indicate that, under the tested conditions, the genes, directly involved in the bioluminescence in P. phosphoreum ANT-2200, are not controlled at a transcriptomic level. Quite obviously, these results demonstrate that the light emission of the strain is not density dependent, which means not under quorum-sensing control. Through this study, we point out that bacterial-bioluminescence regulation should not, from now on, be always linked with the quorum-sensing control.

Dataset Information

Regulation of Bioluminescence in Photobacterium leiognathi Strain KNH6.

Publications

Regulation of Bioluminescence in Photobacterium leiognathi Strain KNH6.

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