Microorganisms can derive energy from dissimilatory sulfate reduction, a process that drives the biogeochemical sulfur cycle and is tightly linked to carbon, nitrogen and metal cycling. Recent metagenomic surveys greatly expanded the diversity of microorganisms that possess the genomic potential for sulfate reduction, highlighting our incomplete understanding of this functional group. In the wake of these studies, an energy metabolism based on the dissimilation of sulfur compounds was proposed for members of the globally distributed and abundant phylum Acidobacteriota. However, fundamental aspects of their ecophysiology are still unknown.

To disentangle the physiology of sulfur compound-dissimilating Acidobacteriota, we followed sulfur-cycling in a long-term continuous culture that was consecutively exposed to oxic and anoxic conditions over a period of more than 200 days. Genome-centric metatranscriptomics embedded into controlled bioreactor operation revealed the unique metabolic flexibility of a representative acidobacterium to switch from sulfate reduction under anoxic conditions to aerobic respiration when oxygen was available as electron acceptor, providing experimental evidence that facultatively anaerobic sulfate-reducing bacteria exist within the Acidobacteriota. This versatile acidobacterium utilized pectin polysaccharides during both sulfate reduction and aerobic respiration. The combination of facultative anaerobiosis and polysaccharide degradation suggested an unprecedented metabolic versatility among sulfate reducers.

These results break three central dogmas in microbiology: sulfate reduction and aerobic respiration are not mutually exclusive in the same organism, sulfate reducers can mineralize organic polymers, and the anaerobic mineralization of complex organic matter is not necessarily a multi-step process involving different microbial guilds but can be accomplished by one microorganism.