Abstract

Methanol is often considered as a non-competitive substrate for methanogenic archaea, but an increasing number of sulfate-reducing microorganisms (SRMs) have been reported to be capable of respiring with methanol as an electron donor. A better understanding of the fate of methanol in natural or artificial anaerobic systems thus requires knowledge of the methanol dissimilation by SRMs. In this study, we describe the growth kinetics and sulfur isotope effects of Desulfovibrio carbinolicus, a methanol-oxidizing sulfate-reducing deltaproteobacterium, together with its genome sequence and annotation. D. carbinolicus can grow with a series of alcohols from methanol to butanol. Compared to longer-chain alcohols, however, specific growth and respiration rates decrease by several fold with methanol as an electron donor. Larger sulfur isotope fractionation accompanies slowed growth kinetics, indicating low chemical potential at terminal reductive steps of respiration. In a medium containing both ethanol and methanol, D. carbinolicus does not consume methanol even after the cessation of growth on ethanol. Among the two known methanol dissimilatory systems, the genome of D. carbinolicus contains the genes coding for alcohol dehydrogenase but lacks enzymes analogous to methanol methyltransferase. We analyzed the genomes of 52 additional species of sulfate-reducing bacteria that have been tested for methanol oxidation. There is no apparent relationship between phylogeny and methanol metabolizing capacity, but most gram-negative methanol oxidizers grow poorly, and none carry homologs for methyltransferase (mtaB). Although the amount of available data is limited, it is notable that more than half of the known gram-positive methanol oxidizers have both enzymatic systems, showing enhanced growth relative to the SRMs containing only alcohol dehydrogenase genes. Thus, physiological, genomic, and sulfur isotopic results suggest that D. carbinolicus and close relatives have the ability to metabolize methanol but likely play a limited role in methanol degradation in most natural environments.

Highlights

  • Sulfate-reducing microorganisms (SRMs) utilize a great variety of organic compounds as an electron donor for energy production, being responsible for most of the terminal carbon mineralization in anoxic environments where sulfate is available [1]

  • Their growth rates are usually slower than those of methanogenic microorganisms at high methanol concentrations, but sulfate-reducing microorganisms (SRMs) have been reported to outcompete methanogens for methanol, where the environmental conditions such as methanol concentration or temperature seem more favorable for SRMs [10,11,12,13]

  • The growth of D. carbinolicus began after a short lag period and ended within 4 days with ethanol, n-propanol, and n-butanol as a sole electron donor (Fig 1A)

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Summary

Introduction

Sulfate-reducing microorganisms (SRMs) utilize a great variety of organic compounds as an electron donor for energy production, being responsible for most of the terminal carbon mineralization in anoxic environments where sulfate is available [1]. Less common, several species of SRMs are capable of oxidizing methanol ([3,4,5,6,7,8,9] and references therein). Their growth rates are usually slower than those of methanogenic microorganisms at high methanol concentrations, but SRMs have been reported to outcompete methanogens for methanol, where the environmental conditions such as methanol concentration or temperature seem more favorable for SRMs [10,11,12,13]. While a role for SRMs in methanol-containing environments has been shown, knowledge about their underlying physiology remains limited

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