Abstract
Fermentation and dissimilatory manganese (Mn) reduction are inter-related metabolic processes that microbes can perform in anoxic environments. Fermentation is less energetically favorable and is often not considered to compete for organic carbon with dissimilatory metal reduction. Therefore, the aim of our study was to investigate the outcome of the competition for lactate between fermentation and Mn oxide (birnessite) reduction in a mixed microbial community. A birnessite reducing enrichment culture was obtained from activated sludge with lactate and birnessite as the substrates. This enrichment was further used to test how various birnessite activities (0, 10, 20, and 40 mM) affected the rates of fermentation and metal reduction, as well as community composition. Increased birnessite activity led to a decrease of lactate consumption rate. Acetate and propionate were the main products. With increasing birnessite activity, the propionate/acetate ratio decreased from 1.4 to 0.47. Significant CO2 production was detected only in the absence of birnessite. In its presence, CO2 concentrations remained close to the background since most of the CO2 produced in these experiments was recovered as MnCO3. The Mn reduction efficiency (Mn(II) produced divided by birnessite added) was the highest at 10 mM birnessite added, where about 50% of added birnessite was reduced to Mn(II), whereas at 20 and 40 mM approximately 21 and 16% was reduced. The decreased birnessite reduction efficiency at higher birnessite activities points to inhibition by terminal electron acceptors and/or its toxicity which was also indicated by retarded lactate oxidation and decreased concentrations of microbial metabolites. Birnessite activity strongly affected microbial community structure. Firmicutes and Bacteroidetes were the most abundant phyla at 0 mM of birnessite. Their abundance was inversely correlated with birnessite concentration. The relative sequence abundance of Proteobacteria correlated with birnessite concentrations. Most of the enriched populations were involved in lactate/acetate or amino acid fermentation and the only previously known metal reducing genus detected was related to Shewanella sp. The sequencing data confirmed that lactate consumption coupled to metal reduction was only one of the processes occurring and did not outcompete fermentation processes.
Highlights
Microbial dissimilatory reduction of mineral oxides such as iron (Fe) and manganese (Mn) hydroxides influences carbon cycling as well as speciation of redox sensitive metals in the environment
Birnessite was used as the only electron acceptor (4.8 g L−1 equivalent to a birnessite activity of 21.5 mM) during enrichment, and lactate (40 mM) was supplied as the only electron donor
The culture was transferred into a fresh medium with the same initial birnessite activity and lactate concentration
Summary
Microbial dissimilatory reduction of mineral oxides such as iron (Fe) and manganese (Mn) hydroxides influences carbon cycling as well as speciation of redox sensitive metals in the environment. It refers to a process where microbes reduce metals for respiration rather than assimilation. Amongst the microorganisms that can reduce metal oxides, there are organisms that do not conserve energy from this process but still perform this reaction as a sink for electrons These include many fermentative and sulfate reducing Bacteria and Archaea (Lovley, 2013 and references therein). They are capable of reducing insoluble Fe(III) and Mn(IV) oxides (Bretschger et al, 2007; Von Canstein et al, 2008; Kouzuma et al, 2012; Richter et al, 2012), and soluble uranium(VI) (Cologgi et al, 2014) and chromium(VI) (Liu et al, 2002; Gong et al, 2018)
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