<i>Salmonella</i> produces sulfide to compete with <i>Escherichia coli</i> in the gut lumen.

Abstract

Hydrogen sulfide production is a characteristic that distinguishes <i>Salmonella</i> serovars from closely related species, such as <i>Escherichia coli</i>, but its biological significance remains obscure. Here, we show that PhsABC and AsrABC-mediated hydrogen sulfide production by <i>Salmonella enterica</i> serovar (<i>S.</i>) Typhimurium was linked to an increased abundance of <i>Deltaproteobacteria</i> and inhibition of cytochrome <i>bd</i> oxidase-mediated aerobic respiration of <i>Escherichia coli</i> in the murine large intestine. Functional <i>phsABC</i> and <i>asrABC</i> operons provided a growth benefit to <i>S.</i> Typhimurium in the cecum of <i>Enterobacterales-</i>free conventional mice only upon inoculation with commensal <i>E. coli.</i> In gnotobiotic mice engrafted with a defined community of 17 human <i>Clostridia</i> isolates, <i>S.</i> Typhimurium infection inhibited cytochrome <i>bd</i> oxidase-mediated aerobic respiration in <i>E. coli</i> only in the presence of <i>Desulfovibrio piger</i>, a sulfide-producing representative of the <i>Deltaproteobacteria.</i> A <i>S.</i> Typhimurium strain deficient for hydrogen sulfide production (<i>phsA asrA</i> mutant) did not inhibit cytochrome <i>bd</i> oxidase-mediated aerobic respiration in <i>E. coli</i>, even when <i>D. piger</i> was present. Collectively, these data suggest that the <i>phsABC</i> and <i>asrABC</i> operons of <i>Salmonella</i> serovars provide a benefit during competition with closely related bacteria, such as <i>E. coli</i>, by inhibiting cytochrome <i>bd</i> oxidase-mediated aerobic respiration of the commensal.