Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1

ABSTRACT Since the original report that Halomonas sp. strain GFAJ-1 was capable of using arsenic instead of phosphorus to sustain growth, additional studies have been conducted, and GFAJ-1 is now considered a highly arsenic-resistant but phosphorus-dependent bacterium. However, the mechanisms suppor...

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Autores principales:	Shuangju Wu, Lianrong Wang, Rui Gan, Tong Tong, Hao Bian, Zhiqiang Li, Shiming Du, Zixin Deng, Shi Chen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	GFAJ-1 arsenate efflux arsenic resistance genome mapping Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6024cb11997b4891b4b528a7e962743d
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spelling	oai:doaj.org-article:6024cb11997b4891b4b528a7e962743d2021-11-15T16:00:26ZSignature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-110.1128/mBio.00515-182150-7511https://doaj.org/article/6024cb11997b4891b4b528a7e962743d2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00515-18https://doaj.org/toc/2150-7511ABSTRACT Since the original report that Halomonas sp. strain GFAJ-1 was capable of using arsenic instead of phosphorus to sustain growth, additional studies have been conducted, and GFAJ-1 is now considered a highly arsenic-resistant but phosphorus-dependent bacterium. However, the mechanisms supporting the extreme arsenic resistance of the GFAJ-1 strain remain unknown. In this study, we show that GFAJ-1 has multiple distinct arsenic resistance mechanisms. It lacks the genes to reduce arsenate, which is the essential step in the well-characterized resistance mechanism of arsenate reduction coupled to arsenite extrusion. Instead, GFAJ-1 has two arsenic resistance operons, arsH1-acr3-2-arsH2 and mfs1-mfs2-gapdh, enabling tolerance to high levels of arsenate. mfs2 and gapdh encode proteins homologous to Pseudomonas aeruginosa ArsJ and glyceraldehyde-3-phosphate dehydrogenase (GAPDH), respectively, which constitute the equivalent of an As(V) efflux system to catalyze the transformation of inorganic arsenate to pentavalent organoarsenical 1-arseno-3-phosphoglycerate and its subsequent extrusion. Surprisingly, the arsH1-acr3-2-arsH2 operon seems to consist of typical arsenite resistance genes, but this operon is sufficient to confer both arsenite and arsenate resistance on Escherichia coli AW3110 even in the absence of arsenate reductase, suggesting a novel pathway of arsenic detoxification. The simultaneous occurrence of these two unusual detoxification mechanisms enables the adaptation of strain GFAJ-1 to the particularly arsenic-rich environment of Mono Lake. IMPORTANCE Halomonas sp. strain GFAJ-1 was previously reported to use arsenic as a substitute for phosphorus to sustain life under phosphate-limited conditions. Although this claim was later undermined by several groups, how GFAJ-1 can thrive in environments with high arsenic concentrations remains unclear. Here, we determined that this ability can be attributed to the possession of two arsenic detoxification operons, arsH1-acr3-2-arsH2 and mfs1-mfs2-gapdh. mfs2 and gapdh encode proteins homologous to ArsJ and GAPDH in Pseudomonas aeruginosa; these proteins create an arsenate efflux pathway to reduce cellular arsenate accumulation. Interestingly, the combination of acr3-2 with either arsH gene was sufficient to confer resistance to both arsenite and arsenate in E. coli AW3110, even in the absence of arsenate reductase, suggesting a new strategy for bacterial arsenic detoxification. This study concludes that the survival of GFAJ-1 in high arsenic concentrations is attributable to the cooccurrence of these two unusual arsenic detoxification mechanisms.Shuangju WuLianrong WangRui GanTong TongHao BianZhiqiang LiShiming DuZixin DengShi ChenAmerican Society for MicrobiologyarticleGFAJ-1arsenate effluxarsenic resistancegenome mappingMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	GFAJ-1 arsenate efflux arsenic resistance genome mapping Microbiology QR1-502
spellingShingle	GFAJ-1 arsenate efflux arsenic resistance genome mapping Microbiology QR1-502 Shuangju Wu Lianrong Wang Rui Gan Tong Tong Hao Bian Zhiqiang Li Shiming Du Zixin Deng Shi Chen Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1
description	ABSTRACT Since the original report that Halomonas sp. strain GFAJ-1 was capable of using arsenic instead of phosphorus to sustain growth, additional studies have been conducted, and GFAJ-1 is now considered a highly arsenic-resistant but phosphorus-dependent bacterium. However, the mechanisms supporting the extreme arsenic resistance of the GFAJ-1 strain remain unknown. In this study, we show that GFAJ-1 has multiple distinct arsenic resistance mechanisms. It lacks the genes to reduce arsenate, which is the essential step in the well-characterized resistance mechanism of arsenate reduction coupled to arsenite extrusion. Instead, GFAJ-1 has two arsenic resistance operons, arsH1-acr3-2-arsH2 and mfs1-mfs2-gapdh, enabling tolerance to high levels of arsenate. mfs2 and gapdh encode proteins homologous to Pseudomonas aeruginosa ArsJ and glyceraldehyde-3-phosphate dehydrogenase (GAPDH), respectively, which constitute the equivalent of an As(V) efflux system to catalyze the transformation of inorganic arsenate to pentavalent organoarsenical 1-arseno-3-phosphoglycerate and its subsequent extrusion. Surprisingly, the arsH1-acr3-2-arsH2 operon seems to consist of typical arsenite resistance genes, but this operon is sufficient to confer both arsenite and arsenate resistance on Escherichia coli AW3110 even in the absence of arsenate reductase, suggesting a novel pathway of arsenic detoxification. The simultaneous occurrence of these two unusual detoxification mechanisms enables the adaptation of strain GFAJ-1 to the particularly arsenic-rich environment of Mono Lake. IMPORTANCE Halomonas sp. strain GFAJ-1 was previously reported to use arsenic as a substitute for phosphorus to sustain life under phosphate-limited conditions. Although this claim was later undermined by several groups, how GFAJ-1 can thrive in environments with high arsenic concentrations remains unclear. Here, we determined that this ability can be attributed to the possession of two arsenic detoxification operons, arsH1-acr3-2-arsH2 and mfs1-mfs2-gapdh. mfs2 and gapdh encode proteins homologous to ArsJ and GAPDH in Pseudomonas aeruginosa; these proteins create an arsenate efflux pathway to reduce cellular arsenate accumulation. Interestingly, the combination of acr3-2 with either arsH gene was sufficient to confer resistance to both arsenite and arsenate in E. coli AW3110, even in the absence of arsenate reductase, suggesting a new strategy for bacterial arsenic detoxification. This study concludes that the survival of GFAJ-1 in high arsenic concentrations is attributable to the cooccurrence of these two unusual arsenic detoxification mechanisms.
format	article
author	Shuangju Wu Lianrong Wang Rui Gan Tong Tong Hao Bian Zhiqiang Li Shiming Du Zixin Deng Shi Chen
author_facet	Shuangju Wu Lianrong Wang Rui Gan Tong Tong Hao Bian Zhiqiang Li Shiming Du Zixin Deng Shi Chen
author_sort	Shuangju Wu
title	Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1
title_short	Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1
title_full	Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1
title_fullStr	Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1
title_full_unstemmed	Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1
title_sort	signature arsenic detoxification pathways in <italic toggle="yes">halomonas</italic> sp. strain gfaj-1
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/6024cb11997b4891b4b528a7e962743d
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Signature Arsenic Detoxification Pathways in <italic toggle="yes">Halomonas</italic> sp. Strain GFAJ-1

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