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.

Highlights

  • Aromatic compounds and arsenic (As) are both toxic substances that often coexist in the environment (Babich and Davis, 1981; Abernathy et al, 2003)

  • Some microorganisms that engage in aromatic degradation utilize more than one of the above degradation pathways (Donoso et al, 2011; Romero-Silva et al, 2013). 3-HBA and 4-HBA are converted to CO2 and H2O via a series of subsequent catabolic processes

  • DmpB, the key protein of the catechol 2,3-dioxygenase degradation pathway, was up-regulated 4.9-fold (Figure 4B and Supplementary Table S3), and other proteins involved in this degradation pathway, DmpC, DmpH, and MphD, were upregulated; their p-values were all >0.05 (Figure 4B and Supplementary Table S3). These results indicated that 4-HBA could be degraded via the catechol 2,3-dioxygenase degradation pathway in the presence of As(III)

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Summary

Introduction

Aromatic compounds and arsenic (As) are both toxic substances that often coexist in the environment (Babich and Davis, 1981; Abernathy et al, 2003). Microorganisms with the ability to bioremediate these substances provide the potential to be used as an environmental treatment Aromatic compounds, such as benzoate (BA) and its derivative hydroxybenzoates (HBAs), 3HBA and 4-HBA, are widely used in chemical engineering and the food, dyeing industry, and pharmaceutical industries (Nordström and Rasmuson, 2006; Franck and Stadelhofer, 2012; Lennerz et al, 2015). The large amounts of residual aromatic compounds in the environment pose a serious threat to human health (Babich and Davis, 1981; Arutchelvan et al, 2005) Microorganisms such as Stenotrophomonas maltophilia KB2, Cupriavidus necator JMP134, and Burkholderia xenovorans LB400 could utilize BA, 3-HBA, and 4-HBA as carbon sources to support their growth and degrade them from the environment (Urszula et al, 2009; Donoso et al, 2011; Romero-Silva et al, 2013). Some microorganisms that engage in aromatic degradation utilize more than one of the above degradation pathways (Donoso et al, 2011; Romero-Silva et al, 2013). 3-HBA and 4-HBA are converted to CO2 and H2O via a series of subsequent catabolic processes

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