Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase

Jackson, Colin R.; Dugas, Sandra L.

doi:10.1186/1471-2148-3-18

Cited by 109 publications

(37 citation statements)

References 43 publications

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“…The pervasive spread of As resistance genes in microbial lineages at the base of the tree of life (e.g., Gihring et al 2003; Jackson and Dugas 2003), suggests exposure to As in the deep geological past (Chen et al 2017; Tian and Luo 2017). This ancient interplay between life and As resulted in the biological innovation of resistance mechanisms whereby As(V) is reduced with unique cytoplasmic As(V) reductases to As(III), followed by extrusion via specific As(III) cell membrane protein transporters (Rosen 2002; Jackson and Dugas 2003; Cai et al 2009; Dziubinska-Maciaszczyk et al 2011; Rosen et al 2011; Slyemi and Bonnefoy 2012a, b; Zhu et al 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Despite the challenge of As toxicity, a peculiar but polyphyletic group of microorganisms conserve energy from As, by respiring As(V) to As(III) and by oxidizing As(III) back to As(V) in a variety of marine and terrestrial habitats (e.g., Mukhopadhyay et al 2002; Smedley and Kinniburgh 2002; Oremland and Stolz 2003; Rosen 2002; Gihring et al 2003; Jackson and Dugas 2003; Oremland and Stolz 2003; Saltikov and Newman 2003; Malasarn et al 2004; Stauder et al 2005; Silver and Phung 2005; Quéméneur et al 2008; Cai et al 2009; Fu et al 2009; Henke et al 2009; Newman et al 2009; Qin et al 2009; Dyhrman and Haley 2011; Dziubinska-Maciaszczyk et al 2011; Rosen et al 2011; Sánchez-Riego et al 2014; Zhu et al 2014, 2017; Gilhooly et al 2014; Jiang et al 2014; Rascovan et al 2016). …”

Section: Introductionmentioning

confidence: 99%

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Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments

et al. 2018

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The toxicity of arsenic (As) towards life on Earth is apparent in the dense distribution of genes associated with As detoxification across the tree of life. The ability to defend against As is particularly vital for survival in As-rich shallow submarine hydrothermal ecosystems along the Hellenic Volcanic Arc (HVA), where life is exposed to hydrothermal fluids containing up to 3000 times more As than present in seawater. We propose that the removal of dissolved As and phosphorus (P) by sulfide and Fe(III)(oxyhydr)oxide minerals during sediment–seawater interaction, produces nutrient-deficient porewaters containing < 2.0 ppb P. The porewater arsenite-As(III) to arsenate-As(V) ratios, combined with sulfide concentration in the sediment and/or porewater, suggest a hydrothermally-induced seafloor redox gradient. This gradient overlaps with changing high affinity phosphate uptake gene abundance. High affinity phosphate uptake and As cycling genes are depleted in the sulfide-rich settings, relative to the more oxidizing habitats where mainly Fe(III)(oxyhydr)oxides are precipitated. In addition, a habitat-wide low As-respiring and As-oxidizing gene content relative to As resistance gene richness, suggests that As detoxification is prioritized over metabolic As cycling in the sediments. Collectively, the data point to redox control on Fe and S mineralization as a decisive factor in the regulation of high affinity phosphate uptake and As cycling gene content in shallow submarine hydrothermal ecosystems along the HVA.Electronic supplementary materialThe online version of this article (10.1007/s10533-018-0500-8) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments

et al. 2018

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“…Although arsenic is most notorious as a poison threatening human health [1], recent studies suggest that arsenic species may have been involved in the ancestral taming of energy and played a crucial role in early stages in the development of life on Earth [2,3]. Further speculations involve this metalloid in the colonization of extraterrestrial environments containing high arsenic levels [4,5].…”

Section: Introductionmentioning

confidence: 99%

A Tale of Two Oxidation States: Bacterial Colonization of Arsenic-Rich Environments

et al. 2007

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Microbial biotransformations have a major impact on contamination by toxic elements, which threatens public health in developing and industrial countries. Finding a means of preserving natural environments—including ground and surface waters—from arsenic constitutes a major challenge facing modern society. Although this metalloid is ubiquitous on Earth, thus far no bacterium thriving in arsenic-contaminated environments has been fully characterized. In-depth exploration of the genome of the β-proteobacterium Herminiimonas arsenicoxydans with regard to physiology, genetics, and proteomics, revealed that it possesses heretofore unsuspected mechanisms for coping with arsenic. Aside from multiple biochemical processes such as arsenic oxidation, reduction, and efflux, H. arsenicoxydans also exhibits positive chemotaxis and motility towards arsenic and metalloid scavenging by exopolysaccharides. These observations demonstrate the existence of a novel strategy to efficiently colonize arsenic-rich environments, which extends beyond oxidoreduction reactions. Such a microbial mechanism of detoxification, which is possibly exploitable for bioremediation applications of contaminated sites, may have played a crucial role in the occupation of ancient ecological niches on earth.

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“…Finally, the detection of arsenic resistance genes (arsC) in our metagenomic assembly from Pohaku Vents represents an exciting opportunity to investigate arsenic detoxification in microbial mat communities at Lo 'ihi. This enzyme catalyzes the intracellular reduction of arsenate to arsenite, which is then extruded from the cell via an arsenite-specific protein pump (31,32). Meyer-Dombard et al found both arsC and zetaproteobacterial SSU rRNA gene sequences in vent fluids and slide colonization experiments in the arsenic-rich waters at shallow hydrothermal vents at Tutum Bay, Papua New Guinea (33).…”

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confidence: 99%

Quantitative PCR Analysis of Functional Genes in Iron-Rich Microbial Mats at an Active Hydrothermal Vent System (Lō'ihi Seamount, Hawai'i)

Jesser

Fullerton

Hager

et al. 2015

Appl Environ Microbiol

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The chemolithotrophic Zetaproteobacteria represent a novel class of Proteobacteria which oxidize Fe(II) to Fe(III) and are the dominant bacterial population in iron-rich microbial mats. Zetaproteobacteria were first discovered at Lo 'ihi Seamount, located 35 km southeast off the big island of Hawai'i, which is characterized by low-temperature diffuse hydrothermal venting. Novel nondegenerate quantitative PCR (qPCR) assays for genes associated with microbial nitrogen fixation, denitrification, arsenic detoxification, Calvin-Benson-Bassham (CBB), and reductive tricarboxylic acid (rTCA) cycles were developed using selected microbial mat community-derived metagenomes. Nitrogen fixation genes were not detected, but all other functional genes were present. This suggests that arsenic detoxification and denitrification processes are likely cooccurring in addition to two modes of carbon fixation. Two groups of microbial mat community types were identified by terminal restriction fragment length polymorphism (T-RFLP) and were further described based on qPCR data for zetaproteobacterial abundance and carbon fixation mode preference. qPCR variance was associated with mat morphology but not with temperature or sample site. Geochemistry data were significantly associated with sample site and mat morphology. Together, these qPCR assays constitute a functional gene signature for iron microbial mat communities across a broad array of temperatures, mat types, chemistries, and sampling sites at Lo 'ihi Seamount. Deep-sea hydrothermal vents are dynamic and extremely productive biological ecosystems supported by chemosynthetic microbial primary production. In the absence of photosynthesis, microorganisms derive energy via the oxidation of reduced chemicals [e.g., H 2 , H 2 S, Fe(II), and CH 4 ] emitted in hydrothermal fluids (1). In contrast to other strategies for microbial chemosynthesis at hydrothermal vents, iron oxidation has only more recently been studied (2). By weight, iron is the most abundant element in the earth, and it has vast potential as an energy source for microbes via chemolithoautotrophy coupled to Fe(II) oxidation (3). However, iron's ability to act as an electron donor for the biotic fixation of CO 2 in neutrophilic environments is limited by the rapid abiotic oxidation of Fe(II) to Fe(III) in the presence of oxygen (4, 5). Despite the ephemeral nature of iron as an energy source, iron-oxidizing bacteria (FeOB) have been identified in a wide array of freshwater and marine habitats and can flourish at circumneutral deep-sea vents with sharp redox gradients and hydrothermal fluids high in CO 2 and reduced iron (6-9). The recently described Zetaproteobacteria represent a novel class of marine Proteobacteria that are diverse and abundant contributors to deep-sea FeOB communities (10).Zetaproteobacteria were first discovered at iron-rich, low-temperature hydrothermal vents at Lo 'ihi Seamount, HI (2, 11), and have been demonstrated to be significant microbial colonizers of seamounts (10, 12). Lo 'ihi Seamount is a s...

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Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase

Cited by 109 publications

References 43 publications

Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments

Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments

A Tale of Two Oxidation States: Bacterial Colonization of Arsenic-Rich Environments

Quantitative PCR Analysis of Functional Genes in Iron-Rich Microbial Mats at an Active Hydrothermal Vent System (Lō'ihi Seamount, Hawai'i)

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