Metagenomic Analysis Reveals Microbial Interactions at the Biocathode of a Bioelectrochemical System Capable of Simultaneous Trichloroethylene and Cr(VI) Reduction

Bruna Matturro; Marco Zepilli; Agnese Lai; Mauro Majone; Simona Rossetti

doi:10.3389/fmicb.2021.747670

Metagenomic Analysis Reveals Microbial Interactions at the Biocathode of a Bioelectrochemical System Capable of Simultaneous Trichloroethylene and Cr(VI) Reduction

Front Microbiol. 2021 Sep 30:12:747670. doi: 10.3389/fmicb.2021.747670. eCollection 2021.

Authors

Bruna Matturro¹, Marco Zepilli², Agnese Lai², Mauro Majone², Simona Rossetti¹

Affiliations

¹ Water Research Institute, IRSA-CNR, Rome, Italy.
² Department of Chemistry, Sapienza University of Rome, Rome, Italy.

Abstract

Bioelectrochemical systems (BES) are attractive and versatile options for the bioremediation of organic or inorganic pollutants, including trichloroethylene (TCE) and Cr(VI), often found as co-contaminants in the environment. The elucidation of the microbial players' role in the bioelectroremediation processes for treating multicontaminated groundwater is still a research need that attracts scientific interest. In this study, 16S rRNA gene amplicon sequencing and whole shotgun metagenomics revealed the leading microbial players and the primary metabolic interactions occurring in the biofilm growing at the biocathode where TCE reductive dechlorination (RD), hydrogenotrophic methanogenesis, and Cr(VI) reduction occurred. The presence of Cr(VI) did not negatively affect the TCE degradation, as evidenced by the RD rates estimated during the reactor operation with TCE (111±2 μeq/Ld) and TCE/Cr(VI) (146±2 μeq/Ld). Accordingly, Dehalococcoides mccartyi, the primary biomarker of the RD process, was found on the biocathode treating both TCE (7.82E+04±2.9E+04 16S rRNA gene copies g^-1 graphite) and TCE/Cr(VI) (3.2E+07±2.37E+0716S rRNA gene copies g^-1 graphite) contamination. The metagenomic analysis revealed a selected microbial consortium on the TCE/Cr(VI) biocathode. D. mccartyi was the sole dechlorinating microbe with H₂ uptake as the only electron supply mechanism, suggesting that electroactivity is not a property of this microorganism. Methanobrevibacter arboriphilus and Methanobacterium formicicum also colonized the biocathode as H₂ consumers for the CH₄ production and cofactor suppliers for D. mccartyi cobalamin biosynthesis. Interestingly, M. formicicum also harbors gene complexes involved in the Cr(VI) reduction through extracellular and intracellular mechanisms.

Keywords: Cr(VI) reduction; Dehalococcoides mccartyi; Methanobacterium formicicum; Methanobrevibacter arboriphilus; bioelectrochemical remediation; reductive dechlorination.