Anodes Stimulate Anaerobic Toluene Degradation via Sulfur Cycling in Marine Sediments.
Hydrocarbons released during oil spills are persistent in marine sediments due to the absence of suitable electron acceptors below the oxic zone. Here, we investigated an alternative bioremediation strategy to remove toluene, a model monoaromatic hydrocarbon, using a bioanode. Bioelectrochemical reactors were inoculated with sediment collected from a hydrocarbon-contaminated marine site, and anodes were polarized at 0 mV and +300 mV (versus an Ag/AgCl [3 M KCl] reference electrode). The degradation of toluene was directly linked to current generation of up to 301 mA m(-2) and 431 mA m(-2) for the bioanodes polarized at 0 mV and +300 mV, respectively. Peak currents decreased over time even after periodic spiking with toluene. The monitoring of sulfate concentrations during bioelectrochemical experiments suggested that sulfur metabolism was involved in toluene degradation at bioanodes. 16S rRNA gene-based Illumina sequencing of the bulk anolyte and anode samples revealed enrichment with electrocatalytically active microorganisms, toluene degraders, and sulfate-reducing microorganisms. Quantitative PCR targeting the α-subunit of the dissimilatory sulfite reductase (encoded by dsrA) and the α-subunit of the benzylsuccinate synthase (encoded by bssA) confirmed these findings. In particular, members of the family Desulfobulbaceae were enriched concomitantly with current production and toluene degradation. Based on these observations, we propose two mechanisms for bioelectrochemical toluene degradation: (i) direct electron transfer to the anode and/or (ii) sulfide-mediated electron transfer.
Laboratory of Microbial Ecology and Technology, Ghent University, Ghent, Belgium Department of Earth and Environmental Sciences, University of Milano-Bicocca, Milan, Italy.
Matteo
M
Daghio
Laboratory of Microbial Ecology and Technology, Ghent University, Ghent, Belgium.
Eleni
E
Vaiopoulou
Laboratory of Microbial Ecology and Technology, Ghent University, Ghent, Belgium.
Sunil A
SA
Patil
School of Civil Engineering and Geosciences, Newcastle University, Newcastle upon Tyne, United Kingdom.
Ana
A
Suárez-Suárez
School of Civil Engineering and Geosciences, Newcastle University, Newcastle upon Tyne, United Kingdom.
Ian M
IM
Head
Department of Earth and Environmental Sciences, University of Milano-Bicocca, Milan, Italy.
Andrea
http://orcid.org/0000-0003-1279-9940
A
Franzetti
Laboratory of Microbial Ecology and Technology, Ghent University, Ghent, Belgium korneel.rabaey@ugent.be.
Korneel
http://orcid.org/0000-0001-8738-7778
K
Rabaey
D000693:Anaerobiosis; D001673:Biodegradation, Environmental; D019755:Carbon-Carbon Lyases; D020564:Deltaproteobacteria / Q000378:metabolism*; D004566:Electrodes; D019015:Geologic Sediments / Q000382:microbiology*; D006838:Hydrocarbons / Q000378:metabolism; D050885:Hydrogensulfite Reductase / Q000235:genetics / Q000378:metabolism; D059013:Microbial Consortia / Q000502:physiology; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017422:Sequence Analysis, DNA; D013431:Sulfates / Q000378:metabolism; D013455:Sulfur / Q000378:metabolism*; D014050:Toluene / Q000378:metabolism*; D014874:Water Pollutants, Chemical / Q000378:metabolism
D006838:Hydrocarbons; D012336:RNA, Ribosomal, 16S; D013431:Sulfates; D014874:Water Pollutants, Chemical; D014050:Toluene; D013455:Sulfur; D050885:Hydrogensulfite Reductase; D019755:Carbon-Carbon Lyases; C114354:benzylsuccinate synthase