The genus Pseudovibrio contains metabolically versatile bacteria adapted for symbiosis

Abstract

The majority of strains belonging to the genus Pseudovibrio have been isolated from marine invertebrates such as tunicates, corals and particularly sponges, but the physiology of these bacteria is poorly understood. In this study, we analyse for the first time the genomes of two Pseudovibrio strains - FO-BEG1 and JE062. The strain FO-BEG1 is a required symbiont of a cultivated Beggiatoa strain, a sulfide-oxidizing, autotrophic bacterium, which was initially isolated from a coral. Strain JE062 was isolated from a sponge. The presented data show that both strains are generalistic bacteria capable of importing and oxidizing a wide range of organic and inorganic compounds to meet their carbon, nitrogen, phosphorous and energy requirements under both, oxic and anoxic conditions. Several physiological traits encoded in the analysed genomes were verified in laboratory experiments with both isolates. Besides the versatile metabolic abilities of both Pseudovibrio strains, our study reveals a number of open reading frames and gene clusters in the genomes that seem to be involved in symbiont-host interactions. Both Pseudovibrio strains have the genomic potential to attach to host cells, interact with the eukaryotic cell machinery, produce secondary metabolites and supply the host with cofactors.

Figure 1

Consensus tree of nearly full-length 16S rDNA sequences of the Pseudovibrio genus, calculated with nucleotides at positions between 101 and 1405 according to E. coli numbering. Sequences belonging to the Chloroflexaceae have been used as out-group to root the tree. The type strains of the Pseudovibrio genus are shown in bold and the sequences investigated in this study are highlighted in green colour. The symbols behind the sequences indicate the isolation source. The isolation source of ‘Other marine animals’ refers to the sequences of Pseudovibrio sp. s1cb33 and Pseudovibrio sp. B411, which have been isolated from the abalone Haliotis diversicolor and the bryozoan Cellepora pumicosa, respectively, according to the NCBI database. For the sequence Pseudovibrio sp. MKT84 only the information ‘marine animals’ as isolation source was available. The bar represents 1.25% sequence divergence.

Figure 2

Comparative circular map of the Pseudovibrio sp. FO-BEG1 chromosome (A) and the plasmid (B). Most outer lane represents the reciprocal best match (RBM)-shared gene content between FO-BEG1 and JE062. Lane two and three represent all predicted ORFs on the lagging (red) and leading (green) strands. The two inner lanes display the GC-plot and the GC-skew. The red arrow indicates a sequence stretch of 3.4–18.4 kb that could not be closed during sequencing. The bar chart (C) expresses the amino acid percentage identity of each RBM shared gene-content between FO-BEG1 and JE062. The blue bar is representing the FO-BEG1 chromosome and orange the corresponding plasmid.

Figure 3

The nonribosomal peptide synthetase-polyketide synthase (NRPS-PKS) system in Pseudovibrio sp. FO-BEG1 and Escherichia coli strain IHE3034. White arrows represent the genes present in Enterobacteriaceae and strain FO-BEG1; black arrows represent the ORFs present only in either Enterobacteriaceae or FO-BEG1 but presumably involved in the production of colibactin; the gray arrow shows a gene presumably not involved in the synthesis of colibactin. The symbol at ORF PSE_3331 represents a gene fusion of E. coli genes clbG and clbH in FO-BEG1; the symbol at PSE_3324-3321 represents a gene insertion or deletion in strain FO-BEG1 or E. coli IHE3034 respectively.

Figure 4

Operon encoding type III secretion system (T3SS) subunits and effector proteins in Pseudovibrio sp. FO-BEG1. White arrows show annotated homologues of T3SS subunits including the gene name within the arrows; black arrows represent annotated effector homologues; dark gray arrows show annotated genes coding for proteins presumably not involved in the T3SS; light gray arrows show hypothetical proteins with unknown function. The locus is indicated above and below some genes for orientation purposes.

Figure 5

Schematic overview of the possible lifestyles and the physiologic capabilities derived from genetic information from the genomes of Pseudovibrio sp. FO-BEG1 and JE062. On the left hand side, physiologic abilities are depicted that could be used in free-living, oxic and anoxic conditions. On the right hand side, the attached or associated lifestyle is illustrated. The host organism for the associated lifestyle can be represented by a sponge, coral or tunicate. Biofilm formation and aggregation could be performed via, e.g. amyloid-like structures or the adhesive Flp (fimbrial low-molecular-weight protein) pili. Furthermore, the amyloid-like structures could be required for the attachment to host cells. The proposed secretion systems with the potential effector proteins could be involved in prokaryote–eukaryote interactions, influencing the cell machinery of the host. Additionally, both Pseudovibrio strains could supply the host with cofactors like vitamins or synthesize secondary metabolites like TDA as a defence mechanism against other prokaryotes or the host.