Tetrachloroethene Dehalorespiration and Growth of Desulfitobacterium frappieri TCE1 in Strict Dependence on the Activity of Desulfovibrio fructosivorans

Abstract

Tetrachloroethene (PCE) dehalorespiration was investigated in a continuous coculture of the sulfatereducing bacterium Desulfovibrio fructosivorans and the dehalorespiring Desulfitobacterium frappieri TCE1 at different sulfate concentrations and in the absence of sulfate. Fructose (2.5 mM) was the single electron donor, which could be used only by the sulfate reducer. With 2.5 mM sulfate, the dehalogenating strain was outnumbered by the sulfate-reducing bacterium, sulfate reduction was the dominating process, and only trace amounts of PCE were dehalogenated by strain TCE1. With 1 mM sulfate in the medium, complete sulfate reduction and complete PCE dehalogenation to cis-dichloroethene (cis-DCE) occurred. In the absence of sulfate, PCE was also completely dehalogenated to cis-DCE, and the population size of strain TCE1 increased significantly. The results presented here describe for the first time dehalogenation of PCE by a dehalorespiring anaerobe in strict dependence on the activity of a sulfate-reducing bacterium with a substrate that is exclusively used by the sulfate reducer. This interaction was studied under strictly controlled and quantifiable conditions in continuous culture and shown to depend on interspecies hydrogen transfer under sulfate-depleted conditions. Interspecies hydrogen transfer was demonstrated by direct H 2 measurements of the gas phase and by the production of methane after the addition of a third organism, Methanobacterium formicicum.Some published results seem to indicate that dehalogenating and/or dehalorespiring bacteria and sulfate-reducing bacteria often share biotopes that are contaminated with chlorinated compounds. In this context for example, Gerritse et al. (23) reported on the isolation of a Desulfovibrio species (strain SULF1) and a Desulfitobacterium species (strain TCE1; now identified and deposited as Desulfitobacterium frappieri TCE1 [24]) from the same reactor, which was inoculated with a tetrachloroethene (PCE)-contaminated soil slurry. Both strains grew well in the presence of high concentrations of PCE (up to 30 mM) and sulfate (up to 20 mM) as electron acceptors. In another example, Drzyzga et al. (16) demonstrated dehalogenation of 2-and 4-fluorobenzoate by a freshwater coculture under sulfate-reducing conditions. One member of this coculture was identified as a Desulfotomaculum species, which was able to mineralize the aromatic intermediates, whereas the other unidentified strain was proposed to be responsible for the dehalogenation reaction. Because the authors of that study were not successful in separating both strains (only the sporeforming Desulfotomaculum species was obtained after pasteurization), they suggested that a symbiotic relationship between these two strains might have been essential when grown with halogenated compounds as the sole carbon source. Difficulties in separating dehalogenating and sulfate-reducing strains from a coculture were also reported by Mägli et al. (32), who isolated the dichloromethane-degrading Dehalobacterium formicoaceticum ...

Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses

“…This approach of defined syntrophic growth enabled direct experimental measurement of the specific effects of associated bacteria on the growth, activity and gene expression of Dehalococcoides, similar to the approach taken for the study of Syntrophomonas wolfei with Methanospirillum hungatei (Beaty and McInerney, 1989), for the study of D. vulgaris with methanogens (Bryant et al, 1977;Scholten et al, 2007;Stolyar et al, 2007;Walker et al, 2009) and for the study of Desulfovibrio sp. strain SULF1 and Desulfovibrio fructosivorans with a dehalorespiring bacterium Desulfitobacterium frappieri TCE1 (Drzyzga et al, 2001;Drzyzga and Gottschal, 2002). In DE195/DVH and DE195/DVH/MC, the dechlorination rates of DE195 were enhanced 2-to 3-fold over the isolate and cell yields were enhanced in the co-culture by B1.5 times.…”

Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates

“…For our experimental system, segregating metabolic processes eliminates inter-enzyme competition and consequently reduces the accumulation of intermediates, thus accelerating the consumption of substrates that produce growth-inhibiting intermediates. This principle has previously only been supported by anecdotal evidence (de Souza et al, 1998;Møller et al, 1998;Pelz et al, 1999;Drzyzga and Gottschal 2002;Holmes et al, 2006) while direct experimental evidence has so far been lacking, thus reflecting an important gap in our knowledge about the consequences of metabolic specialization on microbial processes.…”

“…Empirical evidence to support this prediction, however, remains anecdotal. For example, while substrate cross-feeding is often observed for the consumption of environmental pollutants that produce toxic and growth-inhibiting intermediates (de Souza et al, 1998;Møller et al, 1998;Pelz et al, 1999;Drzyzga and Gottschal 2002;Holmes et al, 2006), there is no empirical evidence that substrate cross-feeding itself accelerates the consumption of those pollutants.…”

“…Substrate cross-feeding occurs when one cell type partially consumes a primary substrate into a metabolic intermediate and another cell type then further consumes the intermediate. Substrate cross-feeding controls numerous environmentally and economically important microbial processes, including the mineralization of organic carbon (Schink, 1997;McInerney et al, 2009), the degradation of environmental contaminants (de Souza et al, 1998;Møller et al, 1998;Pelz et al, 1999;Drzyzga and Gottschal 2002;Holmes et al, 2006) and the recycling of fixed nitrogen into dinitrogen gas (N 2 ) (Martienssen and Schops, 1999;Van de Pas-Schoonen et al, 2005;Costa et al, 2006). While substrate cross-feeding is frequently observed within natural and engineered microbial communities, its effects on microbial processes are often unclear.…”

Growth of Dehalobacter and Dehalococcoides spp. during Degradation of Chlorinated Ethanes

“…Therefore, in mixed cultures that can fully degrade PCE to ethene, two or more organisms are likely involved. Isolates of the genera Dehalobacter (29,56), Desulfitobacterium (13,21,40,51), Desulfuromonas (50), and Sulfospirillum (37) can grow through the dechlorination of PCE or TCE to cDCE, but dechlorination does not proceed further. Here it has been found that in the WL cultures dechlorination of 1,1,2-TCA proceeds through an analogous situation: 1,1,2-TCA was initially transformed to VC by a Dehalobacter sp., but VC was only degraded by the Dehalococcoides sp., as each organism only grew significantly during the respective dechlorination steps.…”