Anaerobic benzene oxidation in Geotalea daltonii involves activation by methylation and is regulated by the transition state regulator AbrB.

Autor: Bullows JE; Department of Biology, Georgia State University, Atlanta, Georgia, USA., Kanak A; Department of Biology, Georgia State University, Atlanta, Georgia, USA., Shedrick L; Department of Biology, Georgia State University, Atlanta, Georgia, USA., Kiessling C; Department of Biology, Georgia State University, Atlanta, Georgia, USA., Aklujkar M; Department of Microbiology, University of Massachusetts, Amherst, Massachusetts, USA., Kostka J; School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA., Chin K-J; Department of Biology, Georgia State University, Atlanta, Georgia, USA.
Jazyk: angličtina
Zdroj: Applied and environmental microbiology [Appl Environ Microbiol] 2024 Oct 23; Vol. 90 (10), pp. e0085624. Date of Electronic Publication: 2024 Sep 17.
DOI: 10.1128/aem.00856-24
Abstrakt: Benzene is a widespread groundwater contaminant that persists under anoxic conditions. The aim of this study was to more accurately investigate anaerobic microbial degradation pathways to predict benzene fate and transport. Preliminary genomic analysis of Geotalea daltonii strain FRC-32, isolated from contaminated groundwater, revealed the presence of putative aromatic-degrading genes. G. daltonii was subsequently shown to conserve energy for growth on benzene as the sole electron donor and fumarate or nitrate as the electron acceptor. The hbs gene, encoding for 3-hydroxybenzylsuccinate synthase (Hbs), a homolog of the radical-forming, toluene-activating benzylsuccinate synthase (Bss), was upregulated during benzene oxidation in G. daltonii , while the bss gene was upregulated during toluene oxidation. Addition of benzene to the G. daltonii whole-cell lysate resulted in toluene formation, indicating that methylation of benzene was occurring. Complementation of σ 54 - (deficient) E. coli transformed with the bss operon restored its ability to grow in the presence of toluene, revealing bss to be regulated by σ 54 . Binding sites for σ 70 and the transition state regulator AbrB were identified in the promoter region of the σ 54 -encoding gene rpoN, and binding was confirmed. Induced expression of abrB during benzene and toluene degradation caused G. daltonii cultures to transition to the death phase. Our results suggested that G. daltonii can anaerobically oxidize benzene by methylation, which is regulated by σ 54 and AbrB. Our findings further indicated that the benzene, toluene, and benzoate degradation pathways converge into a single metabolic pathway, representing a uniquely efficient approach to anaerobic aromatic degradation in G. daltonii .
Importance: The contamination of anaerobic subsurface environments including groundwater with toxic aromatic hydrocarbons, specifically benzene, toluene, ethylbenzene, and xylene, has become a global issue. Subsurface groundwater is largely anoxic, and further study is needed to understand the natural attenuation of these compounds. This study elucidated a metabolic pathway utilized by the bacterium Geotalea daltonii capable of anaerobically degrading the recalcitrant molecule benzene using a unique activation mechanism involving methylation. The identification of aromatic-degrading genes and AbrB as a regulator of the anaerobic benzene and toluene degradation pathways provides insights into the mechanisms employed by G. daltonii to modulate metabolic pathways as necessary to thrive in anoxic contaminated groundwater. Our findings contribute to the understanding of novel anaerobic benzene degradation pathways that could potentially be harnessed to develop improved strategies for bioremediation of groundwater contaminants.
Competing Interests: The authors declare no conflict of interest.
Databáze: MEDLINE
Externí odkaz: