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A benzene-degrading nitrate-reducing microbial consortium displays aerobic and anaerobic benzene degradation pathways

  • Siavash Atashgahi*
  • , Bastian Hornung
  • , Marcelle J. Van Der Waals
  • , Ulisses Nunes Da Rocha
  • , Floor Hugenholtz
  • , Bart Nijsse
  • , Douwe Molenaar
  • , Rob Van Spanning
  • , Alfons J.M. Stams
  • , Jan Gerritse
  • , Hauke Smidt
  • *Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

In this study, we report transcription of genes involved in aerobic and anaerobic benzene degradation pathways in a benzene-degrading denitrifying continuous culture. Transcripts associated with the family Peptococcaceae dominated all samples (21-36% relative abundance) indicating their key role in the community. We found a highly transcribed gene cluster encoding a presumed anaerobic benzene carboxylase (AbcA and AbcD) and a benzoate-coenzyme A ligase (BzlA). Predicted gene products showed >96% amino acid identity and similar gene order to the corresponding benzene degradation gene cluster described previously, providing further evidence for anaerobic benzene activation via carboxylation. For subsequent benzoyl-CoA dearomatization, bam-like genes analogous to the ones found in other strict anaerobes were transcribed, whereas gene transcripts involved in downstream benzoyl-CoA degradation were mostly analogous to the ones described in facultative anaerobes. The concurrent transcription of genes encoding enzymes involved in oxygenase-mediated aerobic benzene degradation suggested oxygen presence in the culture, possibly formed via a recently identified nitric oxide dismutase (Nod). Although we were unable to detect transcription of Nod-encoding genes, addition of nitrite and formate to the continuous culture showed indication for oxygen production. Such an oxygen production would enable aerobic microbes to thrive in oxygen-depleted and nitrate-containing subsurface environments contaminated with hydrocarbons.

Original languageEnglish
Article number4490
Pages (from-to)1-12
Number of pages12
JournalScientific Reports
Volume8
Issue number1
DOIs
Publication statusPublished - 14 Mar 2018

Funding

This study was supported by a grant of BE-Basic-FES funds from the Dutch Ministry of Economic Affairs. The research of A.J.M. Stams is supported by an ERC grant (project 323009) and the gravitation grant “Microbes for Health and Environment” (project 024.002.002) of the Netherlands Ministry of Education, Culture and Science. F. Hugenholtz was supported by the same gravitation grant (project 024.002.002). B. Hornung is supported by Wageningen University and the Wageningen Institute for Environment and Climate Research (WIMEK) through the IP/OP program Systems Biology (project KB-17-003.02-023).

FundersFunder number
Seventh Framework Programme
Ministerie van Economische Zaken
Wageningen University and Research
European Research Council
Ministerie van Onderwijs, Cultuur en Wetenschap
Microbes for Health and Environment
European Commission323009
IP/OP program Systems BiologyKB-17-003.02-023
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