Abstract
Strains of the Pseudovibrio genus have been detected worldwide, mainly as part of bacterial communities associated with marine invertebrates, particularly sponges. This recurrent association has been considered as an indication of a symbiotic relationship between these microbes and their host. Until recently, the availability of only two genomes, belonging to closely related strains, has limited the knowledge on the genomic and physiological features of the genus to a single phylogenetic lineage. Here we present 10 newly sequenced genomes of Pseudovibrio strains isolated from marine sponges from the west coast of Ireland, and including the other two publicly available genomes we performed an extensive comparative genomic analysis. Homogeneity was apparent in terms of both the orthologous genes and the metabolic features shared amongst the 12 strains. At the genomic level, a key physiological difference observed amongst the isolates was the presence only in strain P. axinellae AD2 of genes encoding proteins involved in assimilatory nitrate reduction, which was then proved experimentally. We then focused on studying those systems known to be involved in the interactions with eukaryotic and prokaryotic cells. This analysis revealed that the genus harbors a large diversity of toxin-like proteins, secretion systems and their potential effectors. Their distribution in the genus was not always consistent with the phylogenetic relationship of the strains. Finally, our analyses identified new genomic islands encoding potential toxin-immunity systems, previously unknown in the genus. Our analyses shed new light on the Pseudovibrio genus, indicating a large diversity of both metabolic features and systems for interacting with the host. The diversity in both distribution and abundance of these systems amongst the strains underlines how metabolically and phylogenetically similar bacteria may use different strategies to interact with the host and find a niche within its microbiota. Our data suggest the presence of a sponge-specific lineage of Pseudovibrio. The reduction in genome size and the loss of some systems potentially used to successfully enter the host, leads to the hypothesis that P. axinellae strain AD2 may be a lineage that presents an ancient association with the host and that may be vertically transmitted to the progeny.
Highlights
The genus Pseudovibrio consists of five type strains: P. denitrificans and P. japonicus, isolated from coastal seawater, P. ascidiaceicola isolated from a marine tunicate, P. axinellae isolated from a marine sponge, and P. hongkongensis isolated from a marine flatworm (Bondarev et al, 2013; Xu et al, 2015)
We performed a comparative genomic analysis including the two publicly available Pseudovibrio FO-BEG1 and JE062 genomes, and we describe the general physiological features of these bacteria, focusing on the traits that are likely to be fundamental for these strains to establish and maintain a successful relationship with the host and secure a place in its microbiota
In this work we present 10 newly sequenced Pseudovibrio genomes, and we performed an extensive comparative genomic analysis including the two other publicly available genomes of strains FO-BEG1 and JE062
Summary
The genus Pseudovibrio consists of five type strains: P. denitrificans and P. japonicus, isolated from coastal seawater, P. ascidiaceicola isolated from a marine tunicate, P. axinellae isolated from a marine sponge, and P. hongkongensis isolated from a marine flatworm (Bondarev et al, 2013; Xu et al, 2015). In addition to being recurrently identified in the sponge microbiota, Pseudovibrio related strains have been reported to be dominant in the culturable bacterial fraction of different marine sponges (Webster and Hill, 2001; Muscholl-Silberhorn et al, 2007; Bauvais et al, 2015) and, it has been suggested that a symbiotic relationship might exist between bacteria of the Pseudovibrio genus and these marine invertebrates (Taylor et al, 2007) In support of this hypothesis bacteria belonging to the Pseudovibrio genus have been found to be the most abundant prokaryotes associated with larvae of the sponge Mycale laxissima, indicating vertical transmission (i.e. direct transmission from the parental line to the progeny) of these microbes within their hosts (Enticknap et al, 2006). These findings appear to indicate that Pseudovibrio do not harm the host, and may even be required for its survival and its health (Webster and Hill, 2001)
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