Simultaneous 3-/4-Hydroxybenzoates Biodegradation and Arsenite Oxidation by Hydrogenophaga sp. H7

Front Microbiol. 2019 Jun 18:10:1346. doi: 10.3389/fmicb.2019.01346. eCollection 2019.

Abstract

Aromatic compounds and arsenic (As) often coexist in the environment. As(III)-oxidizing bacteria can oxidize the more toxic As(III) into the less toxic As(V), and As(V) is easily removed. Microorganisms with the ability to degrade aromatic compounds and oxidize arsenite [As(III)] may have strong potential to remediate co-contaminated water. In this study, a Gram-negative bacterium Hydrogenophaga sp. H7 was shown to simultaneously degrade 3-hydroxybenzoate (3-HBA) or 4-HBA (3-/4-HBA) and oxidize arsenite [As(III)] to arsenate [As(V)] during culture. Notably, the addition of As(III) enhanced the degradation rates of 3-/4-HBA, while the addition of 3-/4-HBA resulted in a slight delay in As(III) oxidation. Use of a 1% bacterial culture in combination with FeCl3 could completely degrade 250 mg/L 3-HBA or 4-HBA and remove 400 μM As(III) from simulated lake water within 28 h. Genomic analysis revealed the presence of As(III) oxidation/resistance genes and two putative 3-/4-HBA degradation pathways (the protocatechuate 4,5-dioxygenase degradation pathway and the catechol 2,3-dioxygenase degradation pathway). Comparative proteomics suggested that strain H7 degraded 4-HBA via the protocatechuate 4,5-dioxygenase degradation pathway in the absence of As(III); however, 4-HBA could be degraded via the catechol 2,3-dioxygenase degradation pathway in the presence of As(III). In the presence of As(III), more NADH was produced by the catechol 2,3-dioxygenase degradation pathway and/or by As(III) oxidation, which explained the enhancement of bacterial 4-HBA degradation in the presence of As(III). In addition, the key gene dmpB, which encodes catechol 2,3-dioxygenase in the catechol 2,3-dioxygenase degradation pathway, was knocked out, which resulted in the disappearance of As(III)-enhanced bacterial 4-HBA degradation from the dmpB mutant strain, which further confirmed that As(III) enhancement of 4-HBA degradation was due to the utilization of the catechol 2,3-dioxygenase pathway. These discoveries indicate that Hydrogenophaga sp. H7 has promise for the application to the removal of aromatic compounds and As co-contamination and reveal the relationship between As oxidation and aromatic compound degradation.

Keywords: Hydrogenophaga; aromatic compound degradation; arsenic; arsenite oxidation; hydroxybenzoates.