Tetrathionate Serves as an Alternative Electron Acceptor in a Denitrifying Bacterium

Tetrathionate is an inorganic sulfur compound, which commonly occurs both in the environment and in the mammalian gut. Several intestinal bacteria have been reported to employ tetrathionate as an electron acceptor for anaerobic respiration, using one of the three characterized enzyme systems, irreversible molybdenum-dependent and octaheme tetrathionate reductases (Ttr and Otr, respectively) or reversible thiosulfate dehydrogenases (Tsd). In addition, polysulfide/thiosulfate reductase homologs (Psr) appear to occasionally function as tetrathionate reductases. The role of tetrathionate respiration in environmental strains remains only poorly studied. Here, we show that the denitrifying Betaproteobacterium Aromatoleum aromaticum is able to grow anaerobically with tetrathionate as an alternative electron acceptor. The process is mediated by an apparent Ttr, which is highly induced in tetrathionate-reducing cells. Moreover, a putative Tsd homolog and a protein complex with similarity to quinone-reducing complexes (Qrc) are produced during growth with tetrathionate. We envisage a scenario in which these three proteins together are involved in tetrathionate reduction or even form a reaction loop to balance the cellular redox state. Phylogenetic analysis revealed that Ttr homologs are widespread across Alpha-, Beta-, and Gammaproteobacteria, which suggests an important, yet underappreciated, physiological role of tetrathionate respiration in environmental bacteria.