Diverse Horizontally-Acquired Gene Clusters Confer Sucrose Utilization to Different Lineages of the Marine Pathogen Photobacterium damselae subsp. damselae.

Saqr Abushattal,Carlos R Osorio,Alba V Barca,Ana Vences

doi:10.3390/genes11111244

Abstract

The ability to metabolize sucrose is a variable trait within the family Vibrionaceae. The marine bacterium Photobacterium damselae subsp. damselae (Pdd), pathogenic for marine animals and humans, is generally described as negative for sucrose utilization (Scr−). Previous studies have reported sucrose-utilizing isolates (Scr+), but the genetic basis of this variable phenotype remains uncharacterized. Here, we carried out the genome sequencing of five Scr+ and two Scr− Pdd isolates and conducted a comparative genomics analysis with sixteen additional Pdd genomes sequenced in previous studies. We identified two different versions of a four-gene cluster (scr cluster) exclusive of Scr+ isolates encoding a PTS system sucrose-specific IIBC component (scrA), a fructokinase (scrK), a sucrose-6-phosphate hydrolase (scrB), and a sucrose operon repressor (scrR). A scrA deletion mutant did not ferment sucrose and was impaired for growth with sucrose as carbon source. Comparative genomics analyses suggested that scr clusters were acquired by horizontal transfer by different lineages of Pdd and were inserted into a recombination hot-spot in the Pdd genome. The incongruence of phylogenies based on housekeeping genes and on scr genes revealed that phylogenetically diverse gene clusters for sucrose utilization have undergone extensive horizontal transfer among species of Vibrio and Photobacterium.

Highlights

The family Vibrionaceae includes a diverse and large number of bacterial species that are ubiquitous in marine habitats
Based on the phylogenetic analyses of the scr clusters of Photobacterium damselae subsp. damselae (Pdd) and other species of the family Vibrionaceae, and on the reconstruction of species phylogenies by using the sequences of eight conserved housekeeping genes, we propose that sucrose utilization in Pdd arose from the horizontal acquisition by different Pdd lineages, of at least two distinct versions of gene clusters from species of the Vibrio and Photobacterium genera
In order to study sucrose utilization in this marine pathogen, we screened a collection of 36 Pdd isolates from diverse geographical origins and isolation sources, for their ability to utilize sucrose on the selective and differential medium thiosulfate citrate bile-salt sucrose (TCBS)

Summary

Introduction

The family Vibrionaceae includes a diverse and large number of bacterial species that are ubiquitous in marine habitats. Some species are recognized as pathogens for marine animals and for humans [1,2]. Their ecological importance in aquatic ecosystems and their high genetic plasticity have fuelled a major research effort on Vibrio, Photobacterium, and other genera of this family [3,4,5,6,7]. Most species exhibit a rapid growth in culture and use a large variety of nutrient sources, and the considerable inter- and intraspecies variability in metabolic and nutritional patterns is explained in part by horizontal transfer of gene functions [8,9,10,11]. In addition to compounds that provide selective properties, TCBS contains 2% sucrose and pH indicators, allowing the differentiation between sucrose fermenters that produce yellow colonies (Scr+ phenotype) and non-fermenters that produce green colonies

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Results

Conclusion