Syntrophic growth of sulfate-reducing bacteria and colorless sulfur bacteria during oxygen limitation

Abstract

Stable co-cultures of the sulfate-reducing bacterium Desulfovibrio desulfuricans PA2805 and the colorless sulfur bacterium Thiobacillus thioparus T5 were obtained in continuous cultures supplied with limiting amounts of lactate and oxygen while sulfate was present in excess. Neither species could grow in pure culture under these conditions. Desulfovibrio could grow only when the oxygen concentration was kept low by Thiobacillus. Zerovalent sulfur (S0) produced by Thiobacillus was preferred over sulfate as electron acceptor by Desulfovibrio, but the affinity for S0 seemed to be rather low. This substrate was more efficiently used when sulfide was present suggesting that S0 is preferably used in the form of polysulfides. Through the use of S0 as electron acceptor the sulfide production per lactate by Desulfovibrio was four times higher than with sulfate as acceptor. Thiobacillus produces less sulfate and more S0 when the amount of sulfide available per oxygen increases. The elevated sulfide production by Desulfovibrio thus resulted in an increase of the S0 production by Thiobacillus, again leading to a further increase of the sulfide production. This positive feedback mechanism stabilizes the syntrophic association. The yield on lactate of Desulfovibrio was doubled in the mixed culture compared with growth on lactate and sulfate in pure culture. This yield increase was attributed to the use of zerovalent sulfur instead of sulfate as electron acceptor. Both organisms were thus shown to benefit from a syntrophic interaction in which lactate was oxidized with oxygen, with a rapid cycling of sulfide and zerovalent sulfur serving the transfer of reducing equivalents between the species. These observations shed some light on the occurrence of colorless sulfur bacteria and sulfate-reducing bacteria at the same depth horizons in microbial mats.