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Natural Merodiploidy of the lux-rib Operon of Photobacterium leiognathi from Coastal Waters of Honshu, Japan ^,

Department of Ecological and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan

Received 28 April 2007/ Accepted 11 June 2007

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 25521^T apparently carries only lux-rib₁. In lnuch.13.1, lelon.2.1, lnuch.21.1, and ATCC 25521^T, 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.

Published ahead of print on 22 June 2007.

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