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Abstract

Bacteria belonging to the Pseudovibrio genus are widespread,
metabolically versatile, and able to thrive as both free-living and
host-associated organisms. Although more than 50 genomes are available,
a comprehensive comparative genomics study to resolve taxonomic
inconsistencies is currently missing. We analyzed all available genomes
and used 552 core genes to perform a robust phylogenomic reconstruction.
This in-depth analysis revealed the divergence of two monophyletic basal
lineages of strains isolated from polyclad flatworm hosts, namely
Pseudovibrio hongkongensis and Pseudovibrio stylochi. These strains have
reduced genomes, lack sulfur-related metabolisms and major biosynthetic
gene clusters, and their environmental distribution appears to be
tightly associated with invertebrate hosts. We show experimentally that
the divergent strains are unable to utilize various sulfur compounds
that in contrast can be utilized by the type strain Pseudovibrio
denitrificans. Our analyses suggest that the lineage leading to these
two strains has been subject to relaxed purifying selection resulting in
great gene loss. Overall genome relatedness indices (OGRI) indicate
substantial differences between the divergent strains and the rest of
the genus. While 16S rRNA gene analyses do not support the establishment
of a different genus for the divergent strains, their substantial
genomic, phylogenomic, and physiological differences strongly suggest a
divergent evolutionary trajectory and the need for their
reclassification. Therefore, we propose the novel genus,
Polycladidabacter gen. nov.Importance The genus Pseudovibrio is commonly
associated with marine invertebrates, which are essential for ocean
health and marine nutrient cycling. Traditionally, the phylogeny of the
genus has been based on 16S rRNA gene analysis. The use of the 16S rRNA
gene or any other single marker gene for robust phylogenetic placement
has recently been questioned. We used a large set of marker genes from
all available Pseudovibrio genomes for in-depth phylogenomic analyses.
We identified divergent monophyletic basal lineages within the
Pseudovibrio genus, including two strains isolated from polyclad
flatworms. These strains showed reduced sulfur metabolisms and
biosynthetic capacities. The phylogenomic analyses revealed distinct
evolutionary trajectories and ecological adaptations that differentiate
the divergent strains from the other Pseudovibrio members and suggest
that they fall into a novel genus. Our data show the importance of
widening the use of phylogenomics for better understanding bacterial
physiology, phylogeny and evolution.