Acetate Degradation at Low pH by the Moderately Acidophilic Sulfate Reducer Acididesulfobacillus acetoxydans gen. nov. sp. nov.

Abstract

In acid drainage environments, biosulfidogenesis by sulfate-reducing bacteria (SRB) attenuates the extreme conditions by enabling the precipitation of metals as their sulfides, and the neutralization of acidity through proton consumption. So far, only a handful of moderately acidophilic SRB species have been described, most of which are merely acidotolerant. Here, a novel species within a novel genus of moderately acidophilic SRB is described, Acididesulfobacillus acetoxydans gen. nov. sp. nov. strain INE, able to grow at pH 3.8. Bioreactor studies with strain INE at optimum (5.0) and low (3.9) pH for growth showed that strain INE alkalinized its environment, and that this was more pronounced at lower pH. These studies also showed the capacity of strain INE to completely oxidize organic acids to CO2, which is uncommon among acidophilic SRB. Since organic acids are mainly in their protonated form at low pH, which increases their toxicity, their complete oxidation may be an acid stress resistance mechanism. Comparative proteogenomic and membrane lipid analysis further indicated that the presence of saturated ether-bound lipids in the membrane, and their relative increase at lower pH, was a protection mechanism against acid stress. Interestingly, other canonical acid stress resistance mechanisms, such as a Donnan potential and increased active charge transport, did not appear to be active.

Acetic acid stress response of the acidophilic sulfate reducer Acididesulfobacillus acetoxydans

“…It could be inferred, therefore, that a higher percentage of the unsaturated straight-chain lipid acids may have converted to 10-methyl branched lipids upon acetic acid exposure, possibly as an adaptation mechanism to maintain cell membrane integrity. Furthermore, at low pH (comparing pH 5.0-3.9) the same pattern in priming precursors and 10-methyl branched FAs was observed in A. acetoxydans (S anchez-Andrea et al, 2022). We speculate that the increase in 10-methyl branched FAs may enhance the fluidity of the lipid bilayer in the acetic acidexposed cells.…”

“…The urea cycle is involved in pH homeostasis through urea hydrolysis which yields two ammonia molecules and a carbamate, subsequently formed ammonia yields ammonium by incorporating a proton. A. acetoxydans does not encode a urease but alternatively can use a putative urea amidolyase (0170‐0171) (Hausinger, 2004; Sánchez‐Andrea et al, 2022). For all different conditions, the urea amidolyase was only slightly expressed; making it unlikely to play a major role.…”

“…Nevertheless, the complete oxidation of organic acids is an uncommon metabolic trait of aSRM. Of the seven fully described and isolated acidophilic sulfate reducing bacteria (aSRB), only Acididesulfobacillus acetoxydans can completely oxidize acetic acid to CO 2 through the oxidative acetyl-CoA pathway (Alazard et al, 2010;Frolov et al, 2017;Mori et al, 2003;Panova et al, 2021;S anchez-Andrea et al, 2013S anchez-Andrea et al, , 2015S anchez-Andrea et al, , 2022. Thus, A. acetoxydans is an excellent model microorganism to study acetic acid stress-relief strategies of aSRB.…”

Glycerol amendment enhances biosulfidogenesis in acid mine drainage-affected areas: An incubation column experiment

“…Recently a novel species representing a novel genus of acidophilic SRB was described, Acididesulfobacillus acetoxydans ( Sánchez-Andrea et al, 2022 ). In previous studies, sequences belonging to this genus was incorrectly classified as uncultured Desulfitobacterium ( Sánchez-Andrea et al, 2013 ) (pH 3.8–6.5, opt 5.0), since both genera branch closely in phylogenetic tree reconstructions.…”

“…An important metabolic feature of A. acetoxydans is its capacity for complete oxidation of organic acids to CO 2 ( Sánchez-Andrea et al, 2022 ). This trait is not commonly found in acidophilic SRB.…”