Lessons from studies of Symbiobacterium thermophilum, a unique syntrophic bacterium

Abstract

Symbiobacterium thermophilum is a syntrophic bacterium whose growth depends on coculture with a cognate Bacillus sp. We have been studying the unique features of S. thermophilum in terms of taxonomy, ecology, genome biology, and physiology. Here we overview current knowledge of this bacterium. Although S. thermophilum shows several physiological properties of Gram-negative bacteria, 16S rRNA gene-based phylogeny indicated that it represents a distinct lineage of Gram-positive bacteria with deep branching between the clades for the high-G+C (Actinobacteria) and the low-G+C (Firmicutes) groups. Ecological study has revealed that S. thermophilum and its relatives are widely distributed in the natural environment, including soil, animal intestines and seawater. A whole genome sequencing study uncovered its unusual features, which overall indicate that this bacterium is a member of Firmicutes despite of its high G+C content (68.7%). The genome appeared to retain fully the genes for primary metabolism, except for carbonic anhydrase. We discovered that carbon dioxide is a marked inducer of the mono-growth of S. thermophilum, and speculated that this is due to a lack of carbonic anhydrase. The lines of evidence suggest that S. thermophilum requires additional conditions for full growth, including not only the supply of an unknown positive factor but also the elimination of oxygen and self-growth inhibitory substances. We conclude that the role of the cognate Bacillus is to establish a complex environment suitable for the growth of S. thermophilum, which is achieved by supplying and removing multiple factors. Understandings of this type of mutualism should provide new insight into microbial physiology as well as the issue of uncultivability.