Microbial contributions to coupled arsenic and sulfur cycling in the acid-sulfide hot spring Champagne Pool, New Zealand

K Hug, Bill MAHER, M Stott, Simon FOSTER, J Moreau

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    Abstract

    Acid-sulfide hot springs are analogs of early Earth geothermal systems where microbial metal (loid) resistance likely first evolved. Arsenic is a metalloid enriched in the acid-sulfide hot spring Champagne Pool (Waiotapu, NewZealand). Arsenic speciation in Champagne Pool follows reaction paths not yet fully understood with respect to biotic contributions and coupling to biogeochemical sulfur cycling. Here we present quantitative arsenic speciation from Champagne Pool, finding arsenite dominant in the pool, rim and outflow channel (55–75% total arsenic), and dithio- and trithioarsenates ubiquitous lypresent as 18–25% total arsenic. In the outflow channel, dimethylmonothioarsenate comprised =9% total arsenic, while on the outflow terrace thioarsenates were present at 55% total arsenic. We also quantified sulfide, thiosulfate, sulfate and elemental sulfur, finding sulfide and sulfate as major species in the pool and outflow terrace, respectively. Elemental sulfur concentration reached a maximum at the terrace. Phylogenetic analysis of 16S rRNA genes from metagenomic sequencing revealed the dominance of Sulfurihydrogenibium at all sites and an increased archaeal population at the rim and outflow channel. Several phylotypes were found closely related to known sulfur-and sulfide-oxidizers, as well as sulfur-and sulfate-reducers. Bioinformatic analysis revealed genes underpinning sulfur redox transformations, consistent with sulfur speciation data, and illustrating a microbial role in sulfur-dependent transformation of arsenite to thioarsenate. Metagenomic analysis also revealed genes encoding for arsenate reductase at all sites, reflecting the ubiquity of thioarsenate and a need for microbial arsenate resistance despite anoxic conditions. Absence of the arsenite oxidase gene, aio, at all sites suggests prioritization of arsenite detoxification over coupling to energy conservation. Finally, detection of methyl arsenic in the outflow channel, in conjunction with increased sequences from Aquificaceae, supports a role for methyltransferase in thermophilic arsenic resistance. Our study highlights microbial contributions to coupled arsenic and sulfur cycling at Champagne Pool, with implications for understanding the evolution of microbial arsenic resistance in sulfidic geothermal systems.
    Original languageEnglish
    Pages (from-to)1-14
    Number of pages14
    JournalFrontiers in Microbiology
    Volume5
    DOIs
    Publication statusPublished - 2014

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    Hot Springs
    Arsenic
    Sulfides
    New Zealand
    Sulfur
    Acids
    Sulfates
    Metagenomics
    Arsenate Reductases
    Metalloids
    Genes
    Thiosulfates
    Methyltransferases
    Computational Biology
    rRNA Genes
    Oxidation-Reduction

    Cite this

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    title = "Microbial contributions to coupled arsenic and sulfur cycling in the acid-sulfide hot spring Champagne Pool, New Zealand",
    abstract = "Acid-sulfide hot springs are analogs of early Earth geothermal systems where microbial metal (loid) resistance likely first evolved. Arsenic is a metalloid enriched in the acid-sulfide hot spring Champagne Pool (Waiotapu, NewZealand). Arsenic speciation in Champagne Pool follows reaction paths not yet fully understood with respect to biotic contributions and coupling to biogeochemical sulfur cycling. Here we present quantitative arsenic speciation from Champagne Pool, finding arsenite dominant in the pool, rim and outflow channel (55–75{\%} total arsenic), and dithio- and trithioarsenates ubiquitous lypresent as 18–25{\%} total arsenic. In the outflow channel, dimethylmonothioarsenate comprised =9{\%} total arsenic, while on the outflow terrace thioarsenates were present at 55{\%} total arsenic. We also quantified sulfide, thiosulfate, sulfate and elemental sulfur, finding sulfide and sulfate as major species in the pool and outflow terrace, respectively. Elemental sulfur concentration reached a maximum at the terrace. Phylogenetic analysis of 16S rRNA genes from metagenomic sequencing revealed the dominance of Sulfurihydrogenibium at all sites and an increased archaeal population at the rim and outflow channel. Several phylotypes were found closely related to known sulfur-and sulfide-oxidizers, as well as sulfur-and sulfate-reducers. Bioinformatic analysis revealed genes underpinning sulfur redox transformations, consistent with sulfur speciation data, and illustrating a microbial role in sulfur-dependent transformation of arsenite to thioarsenate. Metagenomic analysis also revealed genes encoding for arsenate reductase at all sites, reflecting the ubiquity of thioarsenate and a need for microbial arsenate resistance despite anoxic conditions. Absence of the arsenite oxidase gene, aio, at all sites suggests prioritization of arsenite detoxification over coupling to energy conservation. Finally, detection of methyl arsenic in the outflow channel, in conjunction with increased sequences from Aquificaceae, supports a role for methyltransferase in thermophilic arsenic resistance. Our study highlights microbial contributions to coupled arsenic and sulfur cycling at Champagne Pool, with implications for understanding the evolution of microbial arsenic resistance in sulfidic geothermal systems.",
    keywords = "arsenic speciation, thioarsenate, microbialdiversity, hotsprings, microbial arsenic resistance, sulfur cycling, Champagne Pool, NewZealand.",
    author = "K Hug and Bill MAHER and M Stott and Simon FOSTER and J Moreau",
    year = "2014",
    doi = "10.3389/fmicb.2014.00569",
    language = "English",
    volume = "5",
    pages = "1--14",
    journal = "Frontiers in Microbiology",
    issn = "1664-302X",
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    TY - JOUR

    T1 - Microbial contributions to coupled arsenic and sulfur cycling in the acid-sulfide hot spring Champagne Pool, New Zealand

    AU - Hug, K

    AU - MAHER, Bill

    AU - Stott, M

    AU - FOSTER, Simon

    AU - Moreau, J

    PY - 2014

    Y1 - 2014

    N2 - Acid-sulfide hot springs are analogs of early Earth geothermal systems where microbial metal (loid) resistance likely first evolved. Arsenic is a metalloid enriched in the acid-sulfide hot spring Champagne Pool (Waiotapu, NewZealand). Arsenic speciation in Champagne Pool follows reaction paths not yet fully understood with respect to biotic contributions and coupling to biogeochemical sulfur cycling. Here we present quantitative arsenic speciation from Champagne Pool, finding arsenite dominant in the pool, rim and outflow channel (55–75% total arsenic), and dithio- and trithioarsenates ubiquitous lypresent as 18–25% total arsenic. In the outflow channel, dimethylmonothioarsenate comprised =9% total arsenic, while on the outflow terrace thioarsenates were present at 55% total arsenic. We also quantified sulfide, thiosulfate, sulfate and elemental sulfur, finding sulfide and sulfate as major species in the pool and outflow terrace, respectively. Elemental sulfur concentration reached a maximum at the terrace. Phylogenetic analysis of 16S rRNA genes from metagenomic sequencing revealed the dominance of Sulfurihydrogenibium at all sites and an increased archaeal population at the rim and outflow channel. Several phylotypes were found closely related to known sulfur-and sulfide-oxidizers, as well as sulfur-and sulfate-reducers. Bioinformatic analysis revealed genes underpinning sulfur redox transformations, consistent with sulfur speciation data, and illustrating a microbial role in sulfur-dependent transformation of arsenite to thioarsenate. Metagenomic analysis also revealed genes encoding for arsenate reductase at all sites, reflecting the ubiquity of thioarsenate and a need for microbial arsenate resistance despite anoxic conditions. Absence of the arsenite oxidase gene, aio, at all sites suggests prioritization of arsenite detoxification over coupling to energy conservation. Finally, detection of methyl arsenic in the outflow channel, in conjunction with increased sequences from Aquificaceae, supports a role for methyltransferase in thermophilic arsenic resistance. Our study highlights microbial contributions to coupled arsenic and sulfur cycling at Champagne Pool, with implications for understanding the evolution of microbial arsenic resistance in sulfidic geothermal systems.

    AB - Acid-sulfide hot springs are analogs of early Earth geothermal systems where microbial metal (loid) resistance likely first evolved. Arsenic is a metalloid enriched in the acid-sulfide hot spring Champagne Pool (Waiotapu, NewZealand). Arsenic speciation in Champagne Pool follows reaction paths not yet fully understood with respect to biotic contributions and coupling to biogeochemical sulfur cycling. Here we present quantitative arsenic speciation from Champagne Pool, finding arsenite dominant in the pool, rim and outflow channel (55–75% total arsenic), and dithio- and trithioarsenates ubiquitous lypresent as 18–25% total arsenic. In the outflow channel, dimethylmonothioarsenate comprised =9% total arsenic, while on the outflow terrace thioarsenates were present at 55% total arsenic. We also quantified sulfide, thiosulfate, sulfate and elemental sulfur, finding sulfide and sulfate as major species in the pool and outflow terrace, respectively. Elemental sulfur concentration reached a maximum at the terrace. Phylogenetic analysis of 16S rRNA genes from metagenomic sequencing revealed the dominance of Sulfurihydrogenibium at all sites and an increased archaeal population at the rim and outflow channel. Several phylotypes were found closely related to known sulfur-and sulfide-oxidizers, as well as sulfur-and sulfate-reducers. Bioinformatic analysis revealed genes underpinning sulfur redox transformations, consistent with sulfur speciation data, and illustrating a microbial role in sulfur-dependent transformation of arsenite to thioarsenate. Metagenomic analysis also revealed genes encoding for arsenate reductase at all sites, reflecting the ubiquity of thioarsenate and a need for microbial arsenate resistance despite anoxic conditions. Absence of the arsenite oxidase gene, aio, at all sites suggests prioritization of arsenite detoxification over coupling to energy conservation. Finally, detection of methyl arsenic in the outflow channel, in conjunction with increased sequences from Aquificaceae, supports a role for methyltransferase in thermophilic arsenic resistance. Our study highlights microbial contributions to coupled arsenic and sulfur cycling at Champagne Pool, with implications for understanding the evolution of microbial arsenic resistance in sulfidic geothermal systems.

    KW - arsenic speciation

    KW - thioarsenate

    KW - microbialdiversity

    KW - hotsprings

    KW - microbial arsenic resistance

    KW - sulfur cycling

    KW - Champagne Pool

    KW - NewZealand.

    U2 - 10.3389/fmicb.2014.00569

    DO - 10.3389/fmicb.2014.00569

    M3 - Article

    VL - 5

    SP - 1

    EP - 14

    JO - Frontiers in Microbiology

    JF - Frontiers in Microbiology

    SN - 1664-302X

    ER -