Abstract
Methanesulfonic acid (MSA) is a relevant intermediate of the biogeochemical cycle of sulfur and environmental microorganisms assume an important role in the mineralization of this compound. Several methylotrophic bacterial strains able to grow on MSA have been isolated from soil or marine water and two conserved operons, msmABCD coding for MSA monooxygenase and msmEFGH coding for a transport system, have been repeatedly encountered in most of these strains. Homologous sequences have also been amplified directly from the environment or observed in marine metagenomic data, but these showed a base composition (G + C content) very different from their counterparts from cultivated bacteria. The aim of this study was to understand which microorganisms within the coastal surface oceanic microflora responded to MSA as a nutrient and how the community evolved in the early phases of an enrichment by means of metagenome and gene-targeted amplicon sequencing. From the phylogenetic point of view, the community shifted significantly with the disappearance of all signals related to the Archaea, the Pelagibacteraceae and phylum SAR406, and the increase in methylotroph-harboring taxa, accompanied by other groups so far not known to comprise methylotrophs such as the Hyphomonadaceae. At the functional level, the abundance of several genes related to sulfur metabolism and methylotrophy increased during the enrichment and the allelic distribution of gene msmA diagnostic for MSA monooxygenase altered considerably. Even more dramatic was the disappearance of MSA import-related gene msmE, which suggests that alternative transporters must be present in the enriched community and illustrate the inadequacy of msmE as an ecofunctional marker for MSA degradation at sea.
Highlights
It is known that methanesulfonic acid (MSA) has been produced during millennia in the atmosphere by the oxidation of dimethylsulfide (DMS) that escapes from the seawater surface (Andreae, 1986; Hynes, Wine & Semmes, 1986; Mihalopoulos et al, 1992; Koga & Tanaka, 1993; Kelly & Murrell, 1999)
Genes associated to the degradation of methanesulfonic acid have previously been studied in various bacterial isolates and found in several metagenomic studies
A clear G + C-content discrepancy between the former and the latter sequences shows that MSA-degrading strains isolated in the laboratory are not good representatives of the natural communities, especially for marine water
Summary
It is known that methanesulfonic acid (MSA) has been produced during millennia in the atmosphere by the oxidation of dimethylsulfide (DMS) that escapes from the seawater surface (Andreae, 1986; Hynes, Wine & Semmes, 1986; Mihalopoulos et al, 1992; Koga & Tanaka, 1993; Kelly & Murrell, 1999). Several methylotrophic bacterial strains have been isolated that can use MSA as sole source of carbon and energy (Kelly & Baker, 1990; Thompson, Owens & Murrell, 1995; De Marco et al, 2000; De Marco et al, 2004; Baxter et al, 2002; Moosvi et al, 2005b) while other microbes are known to use this molecule just as a sulfur supply (Kelly & Murrell, 1999). An operon (msmABCD) encoding a heteromeric monooxygenase (MSA monooxygenase, or MSAMO) and another operon (msmEFGH ) encoding uptake proteins have been found in several MSA-utilizing strains (De Marco et al, 1999; Baxter et al, 2002; Jamshad et al, 2006; Henriques & De Marco, 2015a; Henriques & De Marco, 2015b) and in a marine bacterium isolated from Western Pacific surface waters (Oh et al, 2010)
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