Syntrophic growth of alkaliphilic anaerobes controlled by ferric and ferrous minerals transformation coupled to acetogenesis

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Redox-active iron minerals can act as energy sources or electron-transferring mediators in microbial syntrophic associations, being important means of interspecies metabolic cooperation in sedimentary environments. Alkaline conditions alter the thermodynamic stability of iron minerals, influencing their availability for interspecies syntrophic interactions. We have modeled anaerobic alkaliphilic microbial associations in ethanol-oxidizing co-culture of an obligate syntroph Candidatus “Contubernalis alkalaceticum” and a facultative lithotroph Geoalkalibacter ferrihydriticus, which is capable of dissimilatory Fe(III) reduction and homoacetogenic oxidation of Fe(II) with CO2. The co-cultures were cultivated with thermodynamically metastable ferric-containing ferrihydrite, or ferrous-containing siderite, or without minerals. Mössbauer spectral analysis revealed the transformation of both minerals to the stable magnetite. In the presence of ferrihydrite, G. ferrihydriticus firstly reduced Fe(III) with ethanol and then switched to syntrophic homoacetogenesis, providing the growth of obligate syntroph on ethanol. The ability of G. ferrihydriticus to accept hydrogen from its syntrophic partner and produce extra acetate from carbonate during ethanol oxidation was confirmed by co-culture growth without minerals. In the presence of siderite, G. ferrihydriticus performed homoacetogenesis using two electron donors simultaneously— siderite and hydrogen. Pieces of evidence for direct and indirect hydrogen-mediated electron exchange between partner organisms were obtained. Relative abundancies of partner organisms and the rate of acetate production by their co-cultures were strongly determined by thermodynamic benefits, which G. ferrihydriticus got from redox transformations of iron minerals. Even the minor growth of G. ferrihydriticus sustained the growth of the syntroph. Accordingly, microbe-to-mineral interactions could represent underestimated drivers of syntrophic interactions in alkaline sedimentary environments.

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This work was supported by the Russian Science Foundation, project No. 17-74-30025 (cultivation experiments and iron minerals analysis), the Ministry of Science and Higher Education of the Russian Federation. Mössbauer analyses and thermodynamic calculations were performed with the support of the RFBR research projects No. 18-32-00349 and No. 18-05-00818 correspondingly.

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Correspondence to Daria G. Zavarzina.

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Zavarzina, D.G., Gavrilov, S.N., Chistyakova, N.I. et al. Syntrophic growth of alkaliphilic anaerobes controlled by ferric and ferrous minerals transformation coupled to acetogenesis. ISME J (2019) doi:10.1038/s41396-019-0527-4

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