Methanogenesis and sulfate-reduction: intertwined ancient metabolic pathways?

Title: Methanogenesis and sulfate-reduction: intertwined ancient metabolic pathways?

Speaker: Marion Jespersen

Affiliation: Max Planck Institute for Marine Microbiology, Bremen, Germany

Abstract:

Hydrogenotrophic methanogens are strictly anaerobic archaea that thrive at the thermodynamic limit of Life and assimilate Sulfur by the direct incorporation of sulfides (e.g. S2-). It was accepted that methanogens cannot perform assimilatory sulfate (SO42-) reduction due to obstacles such as toxic intermediates and energetic barriers. However, Methanothermococcus thermolithotrophicus, a marine thermophile, breaks this dogma: it can grow on SO42- as sole Sulfur source [1]. Here, we investigated how these two ancient pathways, hydrogenotrophic methanogenesis and sulfate reduction, can coexist in this organism.

Using a complementary approach of physiological, biochemical, and structural studies, we elucidated its complete SO42- reduction machinery.

While the first two reactions proceed via an ATP-sulfurylase and APS-kinase, common to other organisms, the further steps are catalysed by non-canonical enzymes. 3'-phosphoadenosine-5'-phosphosulfate (PAPS) released by the APS-kinase is converted into sulfite and 3'-phosphoadenosine-5'-phosphate (PAP) by a new class of PAPS-reductase that shares high similarity with the APS-reductases involved in dissimilatory sulfate-reduction. The generated PAP is efficiently hydrolysed by a PAP-phosphatase that was likely derived from an RNA exonuclease. Finally, the F420-dependent sulfite-reductase converts sulfite to sulfide for cellular assimilation [2, 3]. Fsr is a single peptide composed of a F420H2-oxidase and a novel class of sulfite reductase. Despite a structural architecture like dissimilatory sulfite-reductases, Fsr has a reaction mechanism and cofactor coordination identical to assimilatory sulfite-reductases and provides a plausible picture of a sulfite-reductase prototype.  While metagenomic and metatranscriptomic studies suggest that genes of the sulfate-reduction pathway are present in various methanogens, M. thermolithotrophicus uses a distinct way to assimilate sulfate. Our work suggests that its entire sulfate-assimilation pathway was derived from a “mix-and-match” strategy in which the methanogen acquired assimilatory and dissimilatory enzymes from other microorganisms and shaped them to its physiological needs.

[1] Daniels et al., Applied and Environmental Microbiology, 51, (1986)

[2] Johnson & Mukhopadhyay, Journal of biological chemistry, (2005)

[3] Jespersen, Pierik & Wagner, bioRxiv, (2022)