Obligate sugar oxidation in Mesotoga spp., phylum Thermotogae, in the presence of either elemental sulfur or hydrogenotrophic sulfate‐reducers as electron acceptor

Abstract

Mesotoga prima strain PhosAc3 is a mesophilic representative of the phylum Thermotogae comprising only fermentative bacteria so far. We show that while unable to ferment glucose, this bacterium is able to couple its oxidation to reduction of elemental sulfur. We demonstrate furthermore that M. prima strain PhosAc3 as well as M. prima strain MesG1 and Mesotoga infera are able to grow in syntrophic association with sulfate-reducing bacteria (SRB) acting as hydrogen scavengers through interspecies hydrogen transfer. Hydrogen production was higher in M. prima strain PhosAc3 cells co-cultured with SRB than in cells cultured alone in the presence of elemental sulfur. We propose that the efficient sugar-oxidizing metabolism by M. prima strain PhosAc3 in syntrophic association with a hydrogenotrophic sulfate-reducing bacterium can be extrapolated to all members of the Mesotoga genus. Genome comparison of Thermotogae members suggests that the metabolic difference between Mesotoga and Thermotoga species (sugar oxidation versus fermentation) is mainly due to the absence of the bifurcating [FeFe]-hydrogenase in the former. Such an obligate oxidative process for using sugars, unusual within prokaryotes, is the first reported within the Thermotogae. It is hypothesized to be of primary ecological importance for growth of Mesotoga spp. in the environments that they inhabit.

Genomic analysis of the mesophilic Thermotogae genus Mesotoga reveals phylogeographic structure and genomic determinants of its distinct metabolism

“…Instead Fadhlaoui et al . () showed that Mesotoga spp. prefer to grow in syntrophy with hydrogenotrophic sulfate‐reducing bacteria.…”

“…The Mesotoga genomes and transcriptome also elucidated the genetic background for their distinct energy metabolism compared with thermophilic Thermotogae bacteria, that is, the strict need for sulfur or thiosulfate and no or little H 2 production, but rather H 2 S production unless in co‐culture with a sulfate reducer (Fadhlaoui et al ., ). Fadhlaoui et al .…”

“…Fadhlaoui et al . () suggested that Mesotoga' s inability to ferment sugars is mainly due to its lack of a bifurcating hydrogenase. However, K. olearia also lacks this enzyme and ferments pyruvate, producing large amounts of hydrogen using the homologue of M. prima 's only Fe‐hydrogenase (Pollo et al ., ).…”

“…Mesotoga's core metabolism differs from that of other characterized Thermotogae. While growth of most Thermotogae is stimulated by, but not dependent upon, the presence of thiosulfate, sulfur, or other reduced sulfur compounds in laboratory medium (Ravot et al, 1995;Boileau et al, 2016), reduction of sulfur compounds appears to be essential for growth of Mesotoga in pure culture (Hania et al, 2011;Fadhlaoui et al, 2017). The first description of M. prima (Nesbø et al, 2012) reported that growth was only slightly stimulated by the presence of thiosulfate or sulfur.…”

“…In addition to lower optimal growth temperature (37 C-40 C), Mesotoga's core energy metabolism also differs from that of other characterized thermophilic Thermotogae. For instance, while growth of most thermophilic Thermotogae is stimulated by adding sulfur compounds to the medium (Ravot et al, 1995;Boileau et al, 2016), reduction of sulfur compounds appears to be essential for growth of Mesotoga in pure culture and they produce little or no H 2 (Hania et al, 2011(Hania et al, , 2013Fadhlaoui et al, 2017).…”