A Polysaccharide Biosynthesis Locus in Vibrio parahaemolyticus Important for Biofilm Formation Has Homologs Widely Distributed in Aquatic Bacteria Mainly from <i>Gammaproteobacteria</i>

Abstract

Vibrio parahaemolyticus is a seafood-borne pathogen that poses a great threat to public health worldwide. It is found in either a planktonic cell or a biofilm form in the natural environment. The <i>cps</i> locus has been the only extensively studied polysaccharide biosynthesis gene cluster involved in biofilm formation for this bacterium. In this study, we found that an additional polysaccharide biosynthesis locus, <i>scv</i>, is also necessary for biofilm maturation. The <i>scv</i> locus is composed of two operons, and a loss of their expression leads to a defective biofilm phenotype. The transcription of the <i>scv</i> locus is under the control of a sigma 54-dependent response regulator, ScvE. In contrast, the quorum-sensing regulator AphA stimulates the expression of the <i>cps</i> locus and the <i>scvABCD</i> operon found in the <i>scv</i> locus. Bioinformatic analyses demonstrated that <i>scv</i> loci are divergent and widely distributed among 28 genera, including 26 belonging to the <i>Gammaproteobacteria</i> and 2 within the <i>Alphaproteobacteria</i>. We also determined that all <i>scv</i> locus-positive species are water-dwelling. Some strains of <i>Aeromonas</i>, Aliivibrio salmonicida, Pseudomonas anguilliseptica, Vibrio breoganii, and Vibrio scophthalmi probably acquired <i>scv</i> loci through insertion sequences and/or integrase-mediated horizontal gene transfer. Gene duplication and fusion were also detected in some <i>scv</i> homologs. Together, our results suggest that the genome of V. parahaemolyticus harbors two distinct polysaccharide biosynthesis loci, which may play a role in fine-tuning biofilm development, and that <i>scv</i> loci likely evolved by horizontal gene transfer, gene loss, gene duplication, and fragment fusion. <b>IMPORTANCE</b> Polysaccharides are the major component of biofilms, which provide survival advantages for bacteria in aquatic environments. The seafood-borne pathogen V. parahaemolyticus possesses a functionally uncharacterized polysaccharide biosynthesis locus, <i>scv</i>. We demonstrated that the <i>scv</i> locus is important for biofilm maturation and that <i>scv</i> expression is positively regulated by ScvE. Strains from 148 aquatic bacterial species possess <i>scv</i> homolog loci. These bacterial species belong to 28 genera, most of which belong to the <i>Gammaproteobacteria</i> class. The evolution and diversification of <i>scv</i> loci are likely driven by horizontal gene transfer, gene loss, gene duplication, and fragment fusion. Our results provide new insights into the function and evolution of this widespread polysaccharide biosynthesis locus.