Effects of Sulfate Reduction on Trichloroethene Dechlorination by Dehalococcoides-Containing Microbial Communities

Abstract

In order to elucidate interactions between sulfate reduction and dechlorination, we systematically evaluated the effects of different concentrations of sulfate and sulfide on reductive dechlorination by isolates, constructed consortia, and enrichments containing Dehalococcoides sp. Sulfate (up to 5 mM) did not inhibit the growth or metabolism of pure cultures of the dechlorinator Dehalococcoides mccartyi 195, the sulfate reducer Desulfovibrio vulgaris Hildenborough, or the syntroph Syntrophomonas wolfei. In contrast, sulfide at 5 mM exhibited inhibitory effects on growth of the sulfate reducer and the syntroph, as well as on both dechlorination and growth rates of D. mccartyi. Transcriptomic analysis of D. mccartyi 195 revealed that genes encoding ATP synthase, biosynthesis, and Hym hydrogenase were downregulated during sulfide inhibition, whereas genes encoding metal-containing enzymes involved in energy metabolism were upregulated even though the activity of those enzymes (hydrogenases) was inhibited. When the electron acceptor (trichloroethene) was limiting and an electron donor (lactate) was provided in excess to cocultures and enrichments, high sulfate concentrations (5 mM) inhibited reductive dechlorination due to the toxicity of generated sulfide. The initial cell ratio of sulfate reducers to D. mccartyi (1:3, 1:1, or 3:1) did not affect the dechlorination performance in the presence of sulfate (2 and 5 mM). In contrast, under electron donor limitation, dechlorination was not affected by sulfate amendments due to low sulfide production, demonstrating that D. mccartyi can function effectively in anaerobic microbial communities containing moderate sulfate concentrations (5 mM), likely due to its ability to outcompete other hydrogen-consuming bacteria and archaea.IMPORTANCE Sulfate is common in subsurface environments and has been reported as a cocontaminant with chlorinated solvents at various concentrations. Inconsistent results for the effects of sulfate inhibition on the performance of dechlorination enrichment cultures have been reported in the literature. These inconsistent findings make it difficult to understand potential mechanisms of sulfate inhibition and complicate the interpretation of bioremediation field data. In order to elucidate interactions between sulfate reduction and reductive dechlorination, this study systematically evaluated the effects of different concentrations of sulfate and sulfide on reductive dechlorination by isolates, constructed consortia, and enrichments containing Dehalococcoides sp. This study provides a more fundamental understanding of the competition mechanisms between reductive dechlorination by Dehalococcoides mccartyi and sulfate reduction during the bioremediation process. It also provides insights on the significance of sulfate concentrations on reductive dechlorination under electron donor/acceptor-limiting conditions during in situ bioremediation applications. For example, at a trichloroethene-contaminated site with a high sulfate concentration, proper...

Organohalide-respiringDesulfolunaspecies isolated from marine environments

“…This is similar to some other Deltaproteobacteria [23], but in contrast to D. tiedjei which preferentially performs sulfate reduction over OHR with concomitant down-regulation of rdh gene expression [30]. Moreover, sulfide, an RDase inhibitor in D. tiedjei [64] and Dehalococcoides mccartyi strains [28, 29], did not impact 2,6-DBP debromination by Desulfoluna strains at a concentration of 10 mM (Fig. S9A—F).…”

“…OHRB, and in particular members of the Chloroflexi , are fastidious microbes, and are susceptible to inhibition by oxygen [26], sulfate [27] or sulfide [28, 29]. In the presence of both 3-chlorobenzoate and either sulfate, sulfite or thiosulfate, Desulfomonile tiedjei isolated from sewage sludge preferentially performed sulfur oxyanion reduction [30], and OHR inhibition was suggested to be caused by downregulation of rdh gene expression [30].…”

Organohalide-respiring Desulfoluna species isolated from marine environments

“…This is similar to some other Deltaproteobacteria [23], but in contrast to D. tiedjei which preferentially performs sulfate reduction over OHR with concomitant downregulation of rdh gene expression [30]. Moreover, sulfide, an RDase inhibitor in D. tiedjei [63] and Dehalococcoides mccartyi strains [28,29], did not impact 2,6-DBP debromination by Desulfoluna strains even at a concentration of 10 mM (Fig. S10A-F).…”

“…OHRB, and in particular members of the Chloroflexi, are fastidious microbes, and lack the ability to synthesize corrinoid co-factors de novo [9]. Moreover, many OHRB are susceptible to inhibition by oxygen [26], sulfate [27] or sulfide [28,29]. For example, in the presence of both 3chlorobenzoate and either sulfate, sulfite or thiosulfate, Desulfomonile tiedjei isolated from sewage sludge preferentially performed sulfur oxyanion reduction [30], and OHR inhibition was suggested to be caused by downregulation of rdh gene expression [30].…”

Microbial transformation of organic and inorganic halogen compounds

“…Numerous studies have reported OHR activity and occurrence of OHRB and rdhA genes in marine environments (Ahn et al 2009, Atashgahi et al 2018a, Futagami et al 2009, Liu et al 2017. OHRB, and in particular members of the Chloroflexi, are fastidious microbes, and are susceptible to inhibition by oxygen (Adrian et al 2007), sulfate (May et al 2008) or sulfide (He et al 2005, Mao et al 2017. In the presence of both 3-chlorobenzoate and either sulfate, sulfite or thiosulfate, Desulfomonile tiedjei isolated from sewage sludge preferentially performed sulfur oxyanion reduction (Townsend and Suflita 1997), and OHR inhibition was suggested to be caused by downregulation of rdh gene expression (Townsend and Suflita 1997).…”