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bioRxiv preprint doi: https://doi.org/10.1101/2020.02.03.933291; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Genome-resolved metagenomics and detailed geochemical speciation analyses yield 2 new insights into microbial mercury cycling in geothermal springs 3 4 RUNNING TITLE: Microbial mercury cycling in acid warm springs 5 6 Caitlin M. Gionfriddo1,+*, Matthew B. Stott2, #, Jean F. Power2, Jacob M. Ogorek3, David 7 P. Krabbenhoft3, Ryan Wick4, Kathryn Holt4, Lin-Xing Chen5, Brian C. Thomas5, Jillian 8 F. Banfield1, 5, 6 and John W. Moreau1, ‡ 9 10 1School of Earth Sciences, The University of Melbourne, Parkville, VIC, Australia 11 2GNS Science, Wairakei Research Centre, Taupō, New Zealand 12 3Wisconsin Water Science Center, U.S. Geological Survey, Middleton, WI, USA 13 4Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and 14 Biotechnology Institute, University of Melbourne, Victoria 3010, Australia 15 5Department of Earth and Planetary Science, UC Berkeley, Berkeley, CA, USA 16 6Department of Environmental Science, Policy, and Management, University of California, 17 Berkeley, California 94720, United States 18 19 20 21 22 23 Current affiliations: 24 +Oak Ridge National Laboratory, Biosciences Division, Oak Ridge, TN, USA 25 # School of Biological Sciences, University of Canterbury, Christchurch, New Zealand 26 ‡ School of Geographical and Earth Sciences, University of Glasgow, UK 27 28 *Corresponding author: [email protected] 29 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.03.933291; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 30 ABSTRACT 31 Geothermal systems emit substantial amounts of aqueous, gaseous and methylated 32 mercury, but little is known about microbial influences on mercury speciation. Here we 33 report results from genome-resolved metagenomics and mercury speciation analysis of 34 acid warm springs in the Ngawha Geothermal Field (<55 °C, pH < 4.5), Northland Region, 35 Aotearoa (New Zealand). Our aim was to identify the microorganisms genetically equipped 36 for mercury methylation, demethylation, or Hg(II) reduction to volatile Hg(0) in these 37 springs. Dissolved total and methylated mercury concentrations in two adjacent springs 38 with different mercury speciation ranked among the highest reported from natural sources 39 (250–16000 ng L-1 and 0.5–13.9 ng L-1, respectively). Total solid mercury concentrations 40 in spring sediments ranged from 1273 to 7000 µg g-1. In the context of such ultra-high 41 mercury levels, the geothermal microbiome was unexpectedly diverse, and dominated by 42 acidophilic and mesophilic sulfur- and iron-cycling bacteria, mercury- and arsenic-resistant 43 bacteria, and thermophilic and acidophilic archaea. Integrating microbiome structure and 44 metagenomic potential with geochemical constraints, we constructed a conceptual model 45 for biogeochemical mercury cycling in geothermal springs. The model includes abiotic and 46 biotic controls on mercury speciation, and illustrates how geothermal mercury cycling may 47 couple to microbial community dynamics and sulfur and iron biogeochemistry. 48 49 IMPORTANCE 50 Little is currently known about biogeochemical mercury cycling in geothermal systems. 51 This manuscript presents an important new conceptual model, supported by genome- 52 resolved metagenomic analysis and detailed geochemical measurements. This work 53 provides a framework for studying natural geothermal mercury emissions globally. 54 Specifically, our findings have implications for mercury speciation in wastewaters from 55 geothermal power plants and the potential environmental impacts of microbially and 56 abiotically formed mercury species, particularly where mobilized in spring waters that mix 57 with surface- or ground-waters. Furthermore, in the context of thermophilic origins for 58 microbial mercury volatilisation, this report yields new insights into how such processes 59 may have evolved alongside microbial mercury methylation/demethylation, and the 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.03.933291; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 60 environmental constraints imposed by the geochemistry and mineralogy of geothermal 61 systems. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.03.933291; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 62 Introduction 63 Geothermal springs and fumaroles emit substantial amounts of aqueous and gaseous 64 mercury (Hg) (1). Aqueous Hg concentrations in these systems often exceed 100 ng L-1 65 and total Hg levels can approach 25 µg L-1 (2-4). Despite these ultra-high mercury levels, 66 few studies have examined biotic and abiotic mechanisms for Hg transformations or Hg 67 speciation in geothermal springs. Specifically, the potential for native thermophiles to 68 mediate mercury transformations, i.e., reduction of Hg(II) to Hg(0) or + 69 methylation/demethylation of mercury (to CH3Hg or “MeHg”; or to Hg[II], respectively; 70 (5-7) remains poorly understood. 71 72 Hg species have a high binding affinity to thiols and lipids, causing damage to proteins, 73 enzymes, and nucleic acids. They can inhibit microorganisms at sub-micromolar 74 concentrations (8). Microorganisms living in environments with elevated Hg (>100 ng L- 75 1) commonly possess genes encoding for reduction of Hg(II) to volatile Hg(0), as a means 76 of Hg detoxification (9, 10). The mer operon is used by many bacteria and archaea to 77 detoxify Hg(II), by converting it to volatile Hg(0) (7, 10, 11). Interestingly, mer has a 78 phylogenetic origin in the thermophiles (12, 13). Additionally, microbes equipped with the 79 organomercurial lyase, encoding merB gene as part of the mer-operon, are able to detoxify 80 organic Hg compounds, in tandem with mercuric reductase (MerA), to produce methane 81 (CH4) and Hg(0) (9, 14). Finally, some anaerobic bacteria are suspected to be able to 82 oxidatively demethylate Hg species independent of the mer pathway, producing carbon 83 dioxide (CO2) and Hg(II) (15), although a biochemical pathway has not been identified for 84 mer-independent demethylation. 85 86 The efficiency of microbial methylation of Hg(II) to MeHg is still largely unknown in 87 geothermal spring ecosystems, particularly under acidic conditions (<55 °C, pH < 4.5; (4, 88 5, 16)). However, the hgcAB genes required by microorganisms to methylate Hg (17) have 89 been reported from many environments, including wetland sediments, rice paddy soils, 90 thawing permafrost, hypersaline and hypersulfidic waters, soda lakes, and geothermal 91 systems (16, 18-20). These environments typically host abundant sulfate- and iron- 92 reducing bacteria (Deltaproteobacteria), as well as methanogenic and acetogenic 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.03.933291; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 93 Methanomicrobia (Euryarchaeota), Chloroflexi, and Firmicutes, all of which contain 94 species capable of Hg methylation (18, 21-23). Metagenomic analyses have also identified 95 hgcAB genes in Chrysiogenetes, Atribacteria (candidate phylum OP9), and candidate 96 phylum ACD79 (16). Although Hg methylation is most often associated with sulfate 97 reduction, the existence of environmental triggers or controls on Hg methylation remains 98 poorly understood, as does the evolution and phylogenetic distribution of hgcAB genes. 99 100 By comparison, in non-geothermal environments, elevated Hg concentrations can inhibit 101 microbial Hg methylation (24), and lead to conditions favoring MeHg demethylation (25) 102 or methylation-demethylation cycles (26-28). However, in-depth understanding of Hg 103 methylation in geothermal springs, similarly to acid mine drainage (AMD) (29), has not 104 been established. Conversely, acidophiles in AMD systems have been well studied with 105 respect to potential for metal and sulfur cycling (30), but with less focus on Hg speciation 106 and methylation. Here, we combined metagenomic and geochemical speciation analyses 107 to understand Hg transformations in the context of biogeochemical cycling (e.g., S, Fe) in 108 an acidic warm spring microbiome. In order to understand physicochemical constraints on 109 microbial Hg transformations, we studied Hg speciation across a gradient of environmental 110 factors that can influence microbiome composition and activity. We compare our findings 111 to those of previous geothermal
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