Abstract
Energy conservation via the pathway of dissimilatory sulfate reduction is present in a diverse group of prokaryotes, but is most comprehensively studied in Deltaproteobacteria. In this study, whole-genome microarray analyses were used to provide a model of the energy metabolism of the sulfate-reducing archaeon Archaeoglobus fulgidus, based on comparative analysis of litoautotrophic growth with H2/CO2 and thiosulfate, and heterotrophic growth on lactate with sulfate or thiosulfate. Only 72 genes were expressed differentially between the cultures utilizing sulfate or thiosulfate, whereas 269 genes were affected by a shift in energy source. We identified co-located gene cluster encoding putative lactate dehydrogenases (LDHs; lldD, dld, lldEFG), also present in sulfate-reducing bacteria. These enzymes may take part in energy conservation in A. fulgidus by specifically linking lactate oxidation with APS reduction via the Qmo complex. High transcriptional levels of Fqo confirm an important role of F420H2, as well as a menaquinone-mediated electron transport chain, during heterotrophic growth. A putative periplasmic thiosulfate reductase was identified by specific up-regulation. Also, putative genes for transport of sulfate and sulfite are discussed. We present a model for hydrogen metabolism, based on the probable bifurcation reaction of the Mvh:Hdl hydrogenase, which may inhibit the utilization of Fdred for energy conservation. Energy conservation is probably facilitated via menaquinone to multiple membrane-bound heterodisulfide reductase (Hdr) complexes and the DsrC protein—linking periplasmic hydrogenase (Vht) to the cytoplasmic reduction of sulfite. The ambiguous roles of genes corresponding to fatty acid metabolism induced during growth with H2 are discussed. Putative co-assimilation of organic acids is favored over a homologous secondary carbon fixation pathway, although both mechanisms may contribute to conserve the amount of Fdred needed during autotrophic growth with H2.
Highlights
The sulfate-reducing prokaryotes (SRP) have played a central role in cycling of carbon and sulfur in anoxic environments throughout long periods of Earth’s geological history
Doubling time was more than halved in A. fulgidus when thiosulfate (T-L) was added as terminal electron acceptor instead of sulfate (S-L) during growth with lactate (Figure 1A)
In the present work, a model of the energy metabolism in A. fulgidus for the utilization of lactate and hydrogen with thiosulfate or sulfate as terminal electron acceptors is presented based on transcriptome profiling
Summary
The sulfate-reducing prokaryotes (SRP) have played a central role in cycling of carbon and sulfur in anoxic environments throughout long periods of Earth’s geological history. Reduction of sulfate (SO42−) to sulfide (S2−) in A. fulgidus proceeds via the highly conserved dissimilatory sulfate reduction pathway of the SRP (Peck, 1962; Klenk et al, 1997; Pereira et al, 2011). This was probably acquired by Archaeoglobales via multiple lateral gene transfer events from an early ancestor of clostridial SRP (Klein et al, 2001; Zverlov et al, 2005; Meyer and Kuever, 2007)
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