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

Bruna Matturro,Agnese Lai,Simona Rossetti,Marco Zeppilli,Mauro Majone

doi:10.3389/fmicb.2021.747670

Bruna Matturro, Agnese Lai + Show 3 more

Open Access

https://doi.org/10.3389/fmicb.2021.747670

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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.

Highlights

Trichloroethylene (TCE) is a toxic and persistent anthropogenic pollutant commonly found in groundwater and often detected in the aquifer with other co-contaminants, including heavy metals such as the carcinogenic Cr(VI) (Watts et al, 2015)
The TCE transformation to cis-1,2-dichloroethene and vinyl chloride (VC) up to the harmless ethene occurs via the anaerobic reductive dechlorination (RD) in the presence of an electron donor and through the biological activity of specialized organohalide-respiring bacteria (OHRB; Strycharz et al, 2008; Löffler et al, 2013)
The present study reported the microbial andgenomic characterization of a bioelectrochemical system treating TCE- and TCE/Cr(VI)-contaminated water, allowing to elucidate the microbial interactions occurring at the biofilm growing on the cathode (Figure 7)

Summary

Introduction

Trichloroethylene (TCE) is a toxic and persistent anthropogenic pollutant commonly found in groundwater and often detected in the aquifer with other co-contaminants, including heavy metals such as the carcinogenic Cr(VI) (Watts et al, 2015). Dehalococcoides mccartyi is the sole microorganism capable of performing RD to ethene. Dehalococcoides mccartyi is strictly anaerobic and sensitive to oxygen exposure, incapable of substrate fermentation as a source of electrons, and unable to synthesize corrinoids (i.e., cobalamin), fundamental cofactors for the functionality of RDases (Yan et al, 2016; Yang et al, 2017). These metabolic peculiarities make D. mccartyi growth and RD activity favored within mixed anaerobic consortia where non-dechlorinating microorganisms can supply exogenous cofactors

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