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

Bullows, James E.; Kanak, Alison; Shedrick, Lawrence; Kiessling, Christina; Aklujkar, Muktak; Kostka, Joel; Chin, Kuk-Jeong; Nikel, ed., Pablo Ivan

doi:10.1128/aem.00856-24

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

Journal Article · 23 October 2024 · Applied and Environmental Microbiology

DOI: https://doi.org/10.1128/aem.00856-24 · OSTI ID:2446545

^[1];

^[1]; Shedrick, Lawrence ^[1]; Kiessling, Christina ^[1]; Aklujkar, Muktak ^[2]; Kostka, Joel ^[3];

^[1]; Nikel, ed., Pablo Ivan

Department of Biology, Georgia State University, Atlanta, Georgia, USA
Department of Microbiology, University of Massachusetts, Amherst, Massachusetts, USA
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

ABSTRACT 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.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: FG02-07ER64373

OSTI ID:: 2446545

Journal Information:: Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 10 Vol. 90; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Coschigano, P W; Young, L Y

Degradative capacities and bioaugmentation potential of an anaerobic benzene-degrading bacterium strain DN11

Journal Article · 2007 · Environmental Science and Technology · OSTI ID:20978354

Kasai, Yuki; Kodama, Yumiko; Takahata, Yoh; +2 more

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

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