Abstract
BackgroundUtilizing unique carbohydrates or utilizing them more efficiently help bacteria expand and colonize new niches. Horizontal gene transfer (HGT) of catabolic systems is a powerful mechanism by which bacteria can acquire new phenotypic traits that can increase survival and fitness in different niches. In this work, we examined carbon catabolism diversity among Vibrio parahaemolyticus, a marine species that is also an important human and fish pathogen.ResultsPhenotypic differences in carbon utilization between Vibrio parahaemolyticus strains lead us to examine genotypic differences in this species and the family Vibrionaceae in general. Bioinformatics analysis showed that the ability to utilize d-galactose was present in all V. parahaemolyticus but at least two distinct transporters were present; a major facilitator superfamily (MFS) transporter and a sodium/galactose transporter (SGLT). Growth and genetic analyses demonstrated that SGLT was a more efficient transporter of d-galactose and was the predominant type among strains. Phylogenetic analysis showed that d-galactose gene galM was acquired multiples times within the family Vibrionaceae and was transferred between distantly related species. The ability to utilize d-gluconate was universal within the species. Deletion of eda (VP0065), which encodes aldolase, a key enzyme in the Entner-Doudoroff (ED) pathway, reached a similar biomass to wild type when grown on d-gluconate as a sole carbon source. Two additional eda genes were identified, VPA1708 (eda2) associated with a d-glucuronate cluster and VPA0083 (eda3) that clustered with an oligogalacturonide (OGA) metabolism cluster. EDA2 and EDA3 were variably distributed among the species. A metabolic island was identified that contained citrate fermentation, l-rhamnose and OGA metabolism clusters as well as a CRISPR-Cas system. Phylogenetic analysis showed that CitF and RhaA had a limited distribution among V. parahaemolyticus, and RhaA was acquired at least three times. Within V. parahaemolyticus, two different regions contained the gene for L-arabinose catabolism and most strains had the ability to catabolism this sugar.ConclusionOur data suggest that horizontal transfer of metabolic systems among Vibrionaceae is an important source of metabolic diversity. This work identified four EDA homologues suggesting that the ED pathway plays a significant role in metabolism. We describe previously uncharacterized metabolism islands that were hotspots for the gain and loss of functional modules likely mediated by transposons.
Highlights
Utilizing unique carbohydrates or utilizing them more efficiently help bacteria expand and colonize new niches
Different D-galactose transporters associated with different V. parahaemolyticus isolates Comparative phenotypic growth analysis of RIMD2210633, a clinical strain and UCM-V493, an environmental strain in different carbon sources uncovered significant differences between the two strains in their ability to use different carbon sources (Additional file 1: Table S1)
In V. parahaemolyticus, all strains contain the galactose catabolic cluster, no strain contained a homologue of the MglBAC or the GalP type transporters (Fig. 1a and b)
Summary
Utilizing unique carbohydrates or utilizing them more efficiently help bacteria expand and colonize new niches. In 1996, a highly virulent V. parahaemolyticus serogroup O3:K6 strain emerged in Asia and has since disseminated globally [5]. This pandemic clone was sequenced, strain RIMD2210633, and two type three secretion systems (T3SS), one on each chromosome, designated T3SS-1 and T3SS-2 were identified [8]. Studies have identified at least three variant T3SS-2 systems; T3SS2α present on chromosome 2 and the non-homologous T3SS-2β system present on chromosome 1 or chromosome 2, and T3SS-2γ on chromosome 2 that is closely related to T3SS2β [12,13,14]. T3SS-2γ was identified in strains that are members of the clonal complex ST631, a recent pathogenic clone to emerge in the Northeast USA [12, 15, 16]. A recent study has proposed that T3SS-2α is part of a novel Tn-7 like transposon that has co-opted a mini CRISPR-Cas system to potentially mobilize the entire region [17]
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