Abstract

Agrobacterium tumefaciens GW4 is a heterotrophic arsenite [As(III)]/antimonite [Sb(III)]-oxidizing strain. The As(III) oxidase AioAB is responsible for As(III) oxidation in the periplasm and it is also involved in Sb(III) oxidation in Agrobacterium tumefaciens 5A. In addition, Sb(III) oxidase AnoA and cellular H2O2 are also responsible for Sb(III) oxidation in strain GW4. However, the deletion of aioA increased the Sb(III) oxidation efficiency in strain GW4. In the present study, we found that the cell mobility to Sb(III), ATP and NADH contents and heat release were also increased by Sb(III) and more significantly in the aioA mutant. Proteomics and transcriptional analyses showed that proteins/genes involved in Sb(III) oxidation and resistance, stress responses, carbon metabolism, cell mobility, phosphonate and phosphinate metabolism, and amino acid and nucleotide metabolism were induced by Sb(III) and were more significantly induced in the aioA mutant. The results suggested that Sb(III) oxidation may produce energy. In addition, without periplasmic AioAB, more Sb(III) would enter bacterial cells, however, the cytoplasmic AnoA and the oxidative stress response proteins were significantly up-regulated, which may contribute to the increased Sb(III) oxidation efficiency. Moreover, the carbon metabolism was also activated to generate more energy against Sb(III) stress. The generated energy may be used in Sb transportation, DNA repair, amino acid synthesis, and cell mobility, and may be released in the form of heat.

Highlights

  • Antimony (Sb) is widely present in soil and aquatic systems as a result of natural processes and human activities [1, 2]

  • We found that the deletion of aioA increased Sb(III) oxidation efficiency in strain GW4, and the cellular content of H2O2 was increased in strain GW4-ΔaioA

  • We predicted that the deletion of the periplasm As(III)/Sb(III) oxidase gene aioA may affect other metabolic pathways associated with the Sb(III) detoxification and oxidative stress response in strain GW4

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Summary

Introduction

Antimony (Sb) is widely present in soil and aquatic systems as a result of natural processes and human activities [1, 2]. It can exist in multiple oxidation states, with the most common being antimonite [Sb(III)] and antimonate [Sb(V)] [1]. Due to its affinity for the thiol groups of glutathione and proteins, Sb and its compounds are considered as priority pollutants by the United States Environmental Protection Agency [3] and the European Union [4]. The biogeochemical cycle of this element strongly depends on microbial transformation that affects the toxicity and mobility of antimony species in the environment [5, 6]. PLOS ONE | DOI:10.1371/journal.pone.0172823 February 27, 2017

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