Phylogenetic Analysis of the Incidence ofluxGene Horizontal Transfer inVibrionaceae

Abstract

Horizontal gene transfer (HGT) is thought to occur frequently in bacteria in nature and to play an important role in bacterial evolution, contributing to the formation of new species. To gain insight into the frequency of HGT in Vibrionaceae and its possible impact on speciation, we assessed the incidence of interspecies transfer of the lux genes (luxCDABEG), which encode proteins involved in luminescence, a distinctive phenotype. Three hundred three luminous strains, most of which were recently isolated from nature and which represent 11 Aliivibrio, Photobacterium, and Vibrio species, were screened for incongruence of phylogenies based on a representative housekeeping gene (gyrB or pyrH) and a representative lux gene (luxA). Strains exhibiting incongruence were then subjected to detailed phylogenetic analysis of horizontal transfer by using multiple housekeeping genes (gyrB, recA, and pyrH) and multiple lux genes (luxCDABEG). In nearly all cases, housekeeping gene and lux gene phylogenies were congruent, and there was no instance in which the lux genes of one luminous species had replaced the lux genes of another luminous species. Therefore, the lux genes are predominantly vertically inherited in Vibrionaceae. The few exceptions to this pattern of congruence were as follows: (i) the lux genes of the only known luminous strain of Vibrio vulnificus, VVL1 (ATCC 43382), were evolutionarily closely related to the lux genes of Vibrio harveyi; (ii) the lux genes of two luminous strains of Vibrio chagasii, 21N-12 and SB-52, were closely related to those of V. harveyi and Vibrio splendidus, respectively; (iii) the lux genes of a luminous strain of Photobacterium damselae, BT-6, were closely related to the lux genes of the lux-rib 2 operon of Photobacterium leiognathi; and (iv) a strain of the luminous bacterium Photobacterium mandapamensis was found to be merodiploid for the lux genes, and the second set of lux genes was closely related to the lux genes of the lux-rib 2 operon of P. leiognathi. In none of these cases of apparent HGT, however, did acquisition of the lux genes correlate with phylogenetic divergence of the recipient strain from other members of its species. The results indicate that horizontal transfer of the lux genes in nature is rare and that horizontal acquisition of the lux genes apparently has not contributed to speciation in recipient taxa.Horizontal gene transfer (HGT), the acquisition of genes by a member of one bacterial lineage from another lineage, is widely believed to play a major role in bacterial evolutionary divergence and speciation (29,39,40,46). As a possibly common process, HGT also is thought to result in reticulate evolution, precluding or at least seriously complicating reconstruction of bacterial phylogenies (6, 17). The actual frequency of HGT in nature and its influence on bacterial evolution, however, are controversial; many believe that HGT is uncommon, at best has only minor or infrequent effects on the process of bacterial speciation, and does not prevent reconstruction of ba...

Developmental and Microbiological Analysis of the Inception of Bioluminescent Symbiosis in the Marine FishNuchequula nuchalis(Perciformes: Leiognathidae)

“…Nonetheless, to confirm the identity of these bacteria, we sequenced the luxA gene of strains representative of each strain type (see below) from each larval, juvenile, and adult specimen. The luxA gene sequence distinguishes among all known species of luminous bacteria (e.g., 4,5,26,48,49) and therefore provides a rapid and effective means of confirming species identifications. All examined strains (with the exception described below) were confirmed by this method to be members of P. leiognathi (Table 1).…”

“…This bacterial species had not been isolated from the light organ habitat previously, and its interactions with marine animals often are pathogenic (8,14,22). Whether this instance represents a rare occurrence or a more common interaction is not known, but the presence of V. harveyi in coastal waters where larvae of N. nuchalis occur (49) indicates the opportunity for this bacterium to encounter fish whose nascent light organs are in the process of being colonized. One possibility is that V. harveyi is acquired only infrequently by larvae of N. nuchalis and that the pathogenicity of this bacterium leads to death of the fish; as a consequence, larvae that have taken up this bacterium into their nascent light organs would be short-lived and therefore only rarely found.…”

Broad-Host Range Gene Transporter Particles Produced by Aliivibrio fischeri

“…Although HGT would not be responsible for the speciation of luminous bacteria, it would probably be involved in the diversification of emitting light wavelengths shared at the order level. As is predicted from the sequence data (15,30,35), HGT must have occurred for the spectral diversity in light emission to have evolved. All the factors necessary for the expression of functional genes in phylogenetically distant species must have been transferred.…”

“…Although virioplankton is the most abundant class of plankton in a variety of aquatic habitats (2,12,21,23,30,32,33), studies on its behaviour in the environment are scarce. VLP-mediated transduction among microbes has become of interest to researchers in microbial ecology (12,33,34), because of the possible impact VLPs could have on horizontal gene transfer (HGT).…”

Bacterial luciferase reporters: The Swiss army knife of molecular biology

“…1 Bioluminescent bacteria are mostly marine Gammaproteobacteria of the genera Vibrio, Aliivibrio and Photobacterium. 2 In some cases, these luminescent microorganisms are part of a symbiotic relationship with higher organisms such as the angler fish where they are contained in specialized organs for light production. The requirements for the generation of light are diverse and include attraction of prey and mating partners, repulsion of predators, communication with members of the same species, illumination of the environment and camouflage by counter illumination.…”