Anaerobic oxidation of methane coupled to reductive immobilization of hexavalent chromium by “Candidatus Methanoperedens”

The anaerobic oxidation of methane (AOM) carried out by anaerobic methanotrophic archaea (ANME) plays an important role in mitigating methane emissions from aqueous environments and has applications in bioremediation and wastewater treatment. Previous studies showed that AOM could be coupled to chromate reduction. However, the specific responsible microorganisms and the biochemical mechanisms are unclear. Herein, we showed that a consortium dominated by ANME "Candidatus Methanoperedens" was able to couple AOM to the reduction of Cr(VI) to Cr(III) at a stoichiometry close to the theoretical ratio. Quantitative distribution analysis of Cr(III) products suggested Cr(VI) was predominantly reduced via the extracellular respiratory pathways. Further Cr(III)-targeted fluorescent visualization combined with single-cell electron microscopic imaging suggested that Cr(VI) was reduced by "Ca. Methanoperedens" independently. Biochemical mechanism investigation via proteomic analysis showed proteins for nitrate reduction under nitrate-reducing conditions were significantly downregulated in Cr(VI)-reducing incubation. Instead, many multiheme cytochrome c (MHCs) were among the most upregulated proteins during the Cr(VI) reduction process, suggesting MHC-governed pathways for extracellular Cr(VI) reduction. The significant upregulation of a formate-dependent nitrite reductase during Cr(VI) reduction indicated its potential contribution to the small proportion of Cr(VI) reduction inside cells.