Assimilatory sulfate reduction in the marine methanogen Methanothermococcus thermolithotrophicus

Abstract

Methanothermococcus thermolithotrophicus is the only known methanogen that grows on sulfate as its sole sulfur source, uniquely uniting methanogenesis and sulfate reduction. Here we use physiological, biochemical and structural analyses to provide a snapshot of the complete sulfate reduction pathway of this methanogenic archaeon. We find that later steps in this pathway are catalysed by atypical enzymes. PAPS (3′-phosphoadenosine 5′-phosphosulfate) released by APS kinase is converted into sulfite and 3′-phosphoadenosine 5′-phosphate (PAP) by a PAPS reductase that is similar to the APS reductases of dissimilatory sulfate reduction. A non-canonical PAP phosphatase then hydrolyses PAP. Finally, the F420-dependent sulfite reductase converts sulfite to sulfide for cellular assimilation. While metagenomic and metatranscriptomic studies suggest that the sulfate reduction pathway is present in several methanogens, the sulfate assimilation pathway in M. thermolithotrophicus is distinct. We propose that this pathway was ‘mix-and-matched’ through the acquisition of assimilatory and dissimilatory enzymes from other microorganisms and then repurposed to fill a unique metabolic role.

Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction

“…Here, the transition from sulfite to sulfate reduction and sulfane sulfur oxidation is discussed. Siroheme-containing sulfite reductases are involved in assimilatory and dissimilatory processes and, together with assimilatory nitrite reductases and the Fsr and Dsr-LP proteins from methanogens, part of the siroheme-containing reductases family [ 61 – 63 ]. The simpler version of this family (in some cases including dissimilatory DsrAB proteins) was proposed to have been present before the bacterial and archaeal divide [ 9 , 23 , 24 , 64 ].…”