An ArsR/SmtB Family Member Is Involved in the Regulation by Arsenic of the Arsenite Oxidase Operon in Thiomonas arsenitoxydans

Moinier, Danielle; Slyemi, Djamila; Byrne, Deborah; Lignon, Sabrina; Lebrun, Régine; Talla, Emmanuel; Bonnefoy, Violaine

doi:10.1128/aem.01771-14

Cited by 27 publications

(25 citation statements)

References 60 publications

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“…3) suggests that Sb(III) does not interact with the As(III)-sensing system, which thus far is understood to involve AioX and AioS (51), or at least not at the proficiency necessary to readily detect induction of the aioB::lacZ reporter. The Bonnefoy group has documented similar differential As(III) and Sb(III) regulatory effects on the expression of the Thiomonas arsenitoxydans aioBA-cyc1-aioF-cyc2 operon (52)(53)(54), apparently due to the lack of Sb(III) interaction with the aioBA transcriptional activator in this organism, AioF (55). At present, our understanding of Sb(III) detection and the associated changes to transcriptional profiling is quite poor, but the differential influences of As(III) and Sb(III) on induction of aioB and arsR4 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Arsenite Oxidase Also Functions as an Antimonite Oxidase

Wang

Warelow

Kang

et al. 2015

Appl Environ Microbiol

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e Arsenic and antimony are toxic metalloids and are considered priority environmental pollutants by the U.S. Environmental Protection Agency. Significant advances have been made in understanding microbe-arsenic interactions and how they influence arsenic redox speciation in the environment. However, even the most basic features of how and why a microorganism detects and reacts to antimony remain poorly understood. Previous work with Agrobacterium tumefaciens strain 5A concluded that oxidation of antimonite [Sb(III)] and arsenite [As(III)] required different biochemical pathways. Here, we show with in vivo experiments that a mutation in aioA [encoding the large subunit of As(III) oxidase] reduces the ability to oxidize Sb(III) by approximately one-third relative to the ability of the wild type. Further, in vitro studies with the purified As(III) oxidase from Rhizobium sp. strain NT-26 (AioA shares 94% amino acid sequence identity with AioA of A. tumefaciens) provide direct evidence of Sb(III) oxidation but also show a significantly decreased V max compared to that of As(III) oxidation. The aioBA genes encoding As(III) oxidase are induced by As(III) but not by Sb(III), whereas arsR gene expression is induced by both As(III) and Sb(III), suggesting that detection and transcriptional responses for As(III) and Sb(III) differ. While Sb(III) and As(III) are similar with respect to cellular extrusion (ArsB or Acr3) and interaction with ArsR, they differ in the regulatory mechanisms that control the expression of genes encoding the different Ars or Aio activities. In summary, this study documents an enzymatic basis for microbial Sb(III) oxidation, although additional Sb(III) oxidation activity also is apparent in this bacterium. T he metalloids arsenic (As) and antimony (Sb) are members of group 15 of the periodic table and are ubiquitous in the environment. Both are poisonous and have oxidation states of Ϫ3, 0, ϩ3, and ϩ5, with the last two being the most prevalent in the environment (1-5). The release of both As and Sb into the environment can occur either naturally or anthropogenically (e.g., mining), and both are considered by the U.S. Environmental Protection Agency to be priority environmental pollutants (6), with maximum drinking water standards of 10 ppb and 6 ppb for As and Sb, respectively (7). As has received more publicity due to As poisoning that has occurred and that continues (4, 8). However, Sb has emerged as a major contaminant in environments that contain mine tailings, such as those in China, Australia, New Zealand, and parts of Europe (for example, see references 5 and 9-11).Microorganisms are fundamental to elemental cycling in all environments, and this includes As (12, 13) and presumably Sb, although information for the latter is quite sparse. As cycling has been well documented and at present is thought primarily to involve arsenite [As(III)]Narsenate [As(V)] redox transformations and As methylation and demethylation reactions. As(V) is reduced for detoxification purposes (via ArsC) or respiratory...

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Section: Discussionmentioning

confidence: 99%

Arsenite Oxidase Also Functions as an Antimonite Oxidase

Wang

Warelow

Kang

et al. 2015

Appl Environ Microbiol

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“…In contrast, fully As(III)-induced levels in the ⌬arsR2, ⌬arsR3, and ⌬arsR4 mutants were only 21 to 32% of that in the wild-type cells. This implies that the corresponding ArsR proteins behave in the fashion of a transcription factor, at least with respect to pstS1, departing significantly from the oft-described repressor function of ArsR proteins but possibly similar to the function of AioF, recently described by the Bonnefoy group (49). PhoB is a well-described transcriptional activator of the phosphate stress response (50,51), and we previously demonstrated PhoB1 to serve this role in strain 5A, activating itself and pstS1 (20).…”

Section: Discussionmentioning

confidence: 99%

Regulatory Activities of Four ArsR Proteins in Agrobacterium tumefaciens 5A

Kang

Brame

Jetter

et al. 2016

Appl Environ Microbiol

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ArsR is a well-studied transcriptional repressor that regulates microbe-arsenic interactions. Most microorganisms have an arsR gene, but in cases where multiple copies exist, the respective roles or potential functional overlap have not been explored. We examined the repressors encoded by arsR1 and arsR2 (ars1 operon) and by arsR3 and arsR4 (ars2 operon) in Agrobacterium tumefaciens 5A. ArsR1 and ArsR4 are very similar in their primary sequences and diverge phylogenetically from ArsR2 and ArsR3, which are also quite similar to one another. Reporter constructs (lacZ) for arsR1, arsR2, and arsR4 were all inducible by As(III), but expression of arsR3 (monitored by reverse transcriptase PCR) was not influenced by As(III) and appeared to be linked transcriptionally to an upstream lysR-type gene. Experiments using a combination of deletion mutations and additional reporter assays illustrated that the encoded repressors (i) are not all autoregulatory as is typically known for ArsR proteins, (ii) exhibit variable control of each other's encoding genes, and (iii) exert variable control of other genes previously shown to be under the control of ArsR1. Furthermore, ArsR2, ArsR3, and ArsR4 appear to have an activator-like function for some genes otherwise repressed by ArsR1, which deviates from the well-studied repressor role of ArsR proteins. The differential regulatory activities suggest a complex regulatory network not previously observed in ArsR studies. The results indicate that fine-scale ArsR sequence deviations of the reiterated regulatory proteins apparently translate to different regulatory roles. IMPORTANCEGiven the significance of the ArsR repressor in regulating various aspects of microbe-arsenic interactions, it is important to assess potential regulatory overlap and/or interference when a microorganism carries multiple copies of arsR. This study explores this issue and shows that the four arsR genes in A. tumefaciens 5A, associated with two separate ars operons, encode proteins exhibiting various degrees of functional overlap with respect to autoregulation and cross-regulation, as well as control of other functional genes. In some cases, differences in regulatory activity are associated with only limited differences in protein primary structure. The experiments summarized herein also present evidence that ArsR proteins appear to have activator functions, representing novel regulatory activities for ArsR, previously known only to be a repressor. In reaction to arsenic in their environment, microorganisms orchestrate an organized response that may involve arsenite [As(III)] oxidation, arsenate [As(V)] reduction, or both. These redox reactions serve to detoxify or protect the organism or to generate energy, depending on the organism and the genes involved. Current models depict As(III) being taken up into the cell via aquaglyceroporins (e.g., reviewed in references 1, 2, and 3), where it then interacts with a DNA-binding repressor protein, ArsR, resulting in a conformational change in ArsR and causing it...

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“…Currently, the regulation models of As(III) oxidation have only been reported in the As(III)-oxidizing strains that contain aioXSR in their genomes (Kang et al, 2012a , b ; Liu et al, 2012 ; Li et al, 2013 ; Moinier et al, 2014 ). However, the potential proteins involved in the regulation of As(III) oxidase genes in As(III)-oxidizing strains without aioXSR , such as Halomonas sp.…”

Section: Discussionmentioning

confidence: 99%

“…As opposed to A. tumefaciens 5A, in which aioXSR and aioBA are in the same operon and are transcribed in the same direction (Kang et al, 2012b ; Liu et al, 2012 ), the aioXSR and aioBA are in different operons and are divergently transcribed in Thiomonas arsenitoxydans 3As (Moinier et al, 2014 ). The metalloprotein AioF belonging to the ArsR/SmtB family was found to be able to bind specifically to the regulatory region of the aio operon at two distinct positions (Moinier et al, 2014 ). It involved in the tightly control of the aioBA expression functioning together with AioXSR in T. arsenitoxydans 3As (Moinier et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

“…The metalloprotein AioF belonging to the ArsR/SmtB family was found to be able to bind specifically to the regulatory region of the aio operon at two distinct positions (Moinier et al, 2014 ). It involved in the tightly control of the aioBA expression functioning together with AioXSR in T. arsenitoxydans 3As (Moinier et al, 2014 ). However, the three-component system AioXSR is absent in the genomes of some As(III)-oxidizing bacteria (e.g., Halomonas sp.…”

Section: Introductionmentioning

confidence: 99%

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Regulation of arsenite oxidation by the phosphate two-component system PhoBR in Halomonas sp. HAL1

et al. 2015

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Previously, the expression of arsenite [As(III)] oxidase genes aioBA was reported to be regulated by a three-component regulatory system, AioXSR, in a number of As(III)-oxidizing bacterial strains. However, the regulation mechanism is still unknown when aioXSR genes are absent in some As(III)-oxidizing bacterial genomes, such as in Halomonas sp. HAL1. In this study, transposon mutagenesis and gene knock-out mutation were performed, and two mutants, HAL1-phoR931 and HAL1-▵phoB, were obtained in strain HAL1. The phoR and phoB constitute a two-component system which is responsible for phosphate (Pi) acquisition and assimilation. Both of the mutants showed negative As(III)-oxidation phenotypes in low Pi condition (0.1 mM) but not under normal Pi condition (1 mM). The phoBR complementation strain HAL1-▵phoB-C reversed the mutants' null phenotypes back to wild type status. Meanwhile, lacZ reporter fusions using pCM-lacZ showed that the expression of phoBR and aioBA were both induced by As(III) but were not induced in HAL1-phoR931 and HAL1-▵phoB. Using 15 consensus Pho box sequences, a putative Pho box was found in the aioBA regulation region. PhoB was able to bind to the putative Pho box in vivo (bacterial one-hybrid detection) and in vitro (electrophoretic mobility gel shift assay), and an 18-bp binding sequence containing nine conserved bases were determined. This study provided the evidence that PhoBR regulates the expression of aioBA in Halomonas sp. HAL1 under low Pi condition. The new regulation model further implies the close metabolic connection between As and Pi.

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An ArsR/SmtB Family Member Is Involved in the Regulation by Arsenic of the Arsenite Oxidase Operon in Thiomonas arsenitoxydans

Cited by 27 publications

References 60 publications

Arsenite Oxidase Also Functions as an Antimonite Oxidase

Arsenite Oxidase Also Functions as an Antimonite Oxidase

Regulatory Activities of Four ArsR Proteins in Agrobacterium tumefaciens 5A

Regulation of arsenite oxidation by the phosphate two-component system PhoBR in Halomonas sp. HAL1

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