Genome Analysis of Minibacterium massiliensis Highlights the Convergent Evolution of Water-Living Bacteria

Open Access
Publisher Website
Google Scholar
Abstract
Filtration usually eliminates water-living bacteria. Here, we report on the complete genome sequence of Minibacterium massiliensis, a β-proteobacteria that was recovered from 0.22-μm filtered water used for patients in the hospital. The unexpectedly large 4,110,251-nucleotide genome sequence of M. massiliensis was determined using the traditional shotgun sequencing approach. Bioinformatic analyses shows that the M. massiliensis genome sequence illustrates characteristic features of water-living bacteria, including overrepresentation of genes encoding transporters and transcription regulators. Phylogenomic analysis based on the gene content of available bacterial genome sequences displays a congruent evolution of water-living bacteria from various taxonomic origins, principally for genes involved in energy production and conversion, cell division, chromosome partitioning, and lipid metabolism. This phylogenomic clustering partially results from lateral gene transfer, which appears to be more frequent in water than in other environments. The M. massiliensis genome analyses strongly suggest that water-living bacteria are a common source for genes involved in heavy-metal resistance, antibiotics resistance, and virulence factors. Microorganisms are ubiquitous, found in environments including humans and animals, air, soil, and water, even in extreme conditions. Indeed, we isolated an emerging small bacterium M. massiliensis in hemodialysis water despite microbiological control by filtration and chemicals. Its very small size allowed this bacterium to pass through filters. Decoding of its genome revealed the presence of numerous so-called heavy-metal resistance genes encoding protection against chemicals. The genome also encodes virulence factors and antibiotic resistances. Study of M. massiliensis gene content revealed that it shares many genes with other bacteria in its β-proteobacteria family, but also with many other water-living bacteria from other families. Comparison of the M. massiliensis genome with other completely sequenced genomes indicated that a high fraction of genes (17%) had closest neighbors in water-living bacteria from other families. Such lateral gene transfer was further generalized to all water-living bacteria, which mutualize a higher fraction of their genome than bacteria living in other environments. Water is a privileged ecosystem for the exchange of bacterial genes and the emergence of new combinations of virulence and resistance. As new technologies increase the contact of humans with water, its use for medical and recreational usages has to be thoroughly controlled.