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Metal Transformation by a Novel Pelosinus Isolate from a Subsurface Environment

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INL/JOU-08-14091-Revision-0 Metal Transformation by a Novel Pelosinus Isolate From a Subsurface Environment Allison E. Ray, Peter P. Sheridan, Andrew L. Neal, Yoshiko Fujita, David E. Cummings, Timothy S. Magnuson August 2018 The INL is a U.S. Department of Energy National Laboratory operated by Battelle Energy Alliance INL/JOU-08-14091-Revision-0 Metal Transformation by a Novel Pelosinus Isolate From a Subsurface Environment Allison E. Ray, Peter P. Sheridan, Andrew L. Neal, Yoshiko Fujita, David E. Cummings, Timothy S. Magnuson August 2018 Idaho National Laboratory Idaho Falls, Idaho 83415 http://www.inl.gov Prepared for the U.S. Department of Energy Office of Nuclear Energy Under DOE Idaho Operations Office Contract DE-AC07-05ID14517 fmicb-09-01689 July 25, 2018 Time: 20:42 # 1 ORIGINAL RESEARCH published: xx July 2018 doi: 10.3389/fmicb.2018.01689 1 58 2 59 3 60 4 61 5 62 6 63 7 64 8 65 9 Metal Transformation by a Novel 66 10 67 11 Pelosinus Isolate From a Subsurface 68 12 69 13 Environment 70 14 71 15 Allison E. Ray1,2, Stephanie A. Connon1,3, Andrew L. Neal4†, Yoshiko Fujita2, 72 5 2† 1 16 David E. Cummings , Jani C. Ingram and Timothy S. Magnuson * 73 17 74 1 Department of Biological Sciences, Idaho State University, Pocatello, ID, United States, 2 Bioenergy Technologies, Idaho 18 3 75 Edited by: National Laboratory, Idaho Falls, ID, United States, California Institute of Technology, Pasadena, CA, United States, 19 4 5 76 Pankaj Kumar Arora, Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, United States, Department of Biology, Point Loma 20 77 Babasaheb Bhimrao Ambedkar Nazarene University, San Diego, CA, United States 21 University, India 78 22 79 Reviewed by: The capability of microorganisms to alter metal speciation offers potential for 23 80 Ramprasad E.V.V., the development of new strategies for immobilization of toxic metals in the 24 University of Hyderabad, India 81 25 Bärbel Ulrike Fösel, environment. A metal-reducing microbe, “Pelosinus lilae” strain UFO1, was isolated 82 26 Helmholtz Zentrum München, under strictly anaerobic conditions from an Fe(III)-reducing enrichment established 83 27 Helmholtz-Gemeinschaft Deutscher 84 Forschungszentren (HZ), Germany with uncontaminated soil from the Department of Energy Oak Ridge Field Research 28 85 Center, Tennessee. “P. lilae” UFO1 is a rod-shaped, spore-forming, and Gram-variable 29 *Correspondence: 86 30 Timothy S. Magnuson anaerobe with a fermentative metabolism. It is capable of reducing the humic acid 87 [email protected] 31 analog anthraquinone-2,6-disulfonate (AQDS) using a variety of fermentable substrates 88 † 32 Present address: and H . Reduction of Fe(III)-nitrilotriacetic acid occurred in the presence of lactate as 89 Andrew L. Neal, 2 33 90 Department of Sustainable Soils carbon and electron donor. Ferrihydrite was not reduced in the absence of AQDS. 34 91 and Grassland Systems, Rothamsted Nearly complete reduction of 1, 3, and 5 ppm Cr(VI) occurred within 24 h in suspensions 35 92 Research, Hertfordshire, 8 −1 36 United Kingdom containing 10 cells mL when provided with 10 mM lactate; when 1 mM AQDS was 93 37 Jani C. Ingram, added, 3 and 5 ppm Cr(VI) were reduced to 0.1 ppm within 2 h. Strain UFO1 is a 94 38 Department of Chemistry & novel species within the recently described bacterial genus Pelosinus, having 98.16% 95 39 Biochemistry, Northern Arizona 96 University, Flagstaff, AZ, United States 16S rRNA gene sequence similarity with the most closely related described species, 40 97 T C 41 Pelosinus fermentans R7 . The G C content of the genomic DNA was 38 mol%, 98 Specialty section: T 42 and DNA-DNA hybridization of “P. lilae” UFO1 against P. fermentans R7 indicated an 99 This article was submitted to 43 Microbiotechnology, Ecotoxicology average 16.8% DNA-DNA similarity. The unique phylogenetic, physiologic, and metal- 100 44 and Bioremediation, transforming characteristics of “P. lilae” UFO1 reveal it is a novel isolate of the described 101 45 a section of the journal 102 genus Pelosinus. 46 Frontiers in Microbiology 103 47 Received: 29 December 2017 Keywords: toxic metal reduction, bioremediation, subsurface environment, fermentative bacterium, Pelosinus 104 48 Accepted: 06 July 2018 105 49 Published: xx July 2018 106 50 Citation: INTRODUCTION 107 51 Ray AE, Connon SA, Neal AL, Fujita Y, 108 52 Cummings DE, Ingram JC and The pollution of groundwater by metal and radionuclide contaminants continues to pose a 109 Magnuson TS (2018) Metal 53 clear threat to public health (EPA, 2003), and remediation of subsurface environments is a 110 Transformation by a Novel Pelosinus 54 growing environmental and economic challenge (White et al., 1997; NABIR, 2003). In the 111 Isolate From a Subsurface 55 Environment. United States, the Department of Energy (DOE) has generated 6.4 trillion L of contaminated 112 3 56 Front. Microbiol. 9:1689. groundwater in 5700 distinct plumes and 40 million m of contaminated soil and subsurface 113 57 doi: 10.3389/fmicb.2018.01689 environs as a result of Cold War era nuclear weapons production (USDOE, 1997). After 114 Frontiers in Microbiology | www.frontiersin.org 1 July 2018 | Volume 9 | Article 1689 fmicb-09-01689 July 25, 2018 Time: 20:42 # 2 Ray et al. Metal Transformation by a Pelosinus From a Subsurface Environment 115 petroleum fuel and chlorinated hydrocarbons, metals and phylogenetic analysis of this group common in subsurface 172 116 radionuclides (lead, chromium, arsenic, uranium, strontium- environments. Thus, examining new representatives of this 173 117 90, and tritium) represent the most common contaminants group contributes to a broader understanding of the organisms 174 118 found in soils and groundwater at DOE facilities (Riley et al., involved in the biotransformation of metals in subsurface 175 119 1992). Moreover, metallic and radioactive contaminants cannot environments. 176 120 be biodegraded and often prove to be the most challenging of In situ biological treatment can be less expensive and less 177 121 hazardous wastes at DOE sites (NABIR, 2003). disruptive than traditional ex situ technologies for remediation 178 122 In contrast to organic contaminants that may be completely of metal-contaminated sites, as it relies on indigenous 179 123 oxidized to carbon dioxide and water, remediation of metals is microorganisms to achieve clean-up of hazardous wastes 180 124 more problematic, owing to the fact that the metals cannot be (NABIR, 2003). Examination of the biological potential for 181 125 destroyed, and changes in their oxidation or reduction potential metal reduction among native microorganisms is important for 182 126 often dictate their ultimate environmental fate (Lovley and implementation of successful remediation strategies. However, 183 127 Lloyd, 2000). Generally, the goal of metal remediation is to little is known about the potential for fermentative, Fe(III)- 184 128 limit contaminant mobility. The potential for immobilization reducing subsurface microorganisms to play a role in metal 185 129 of a given metal in the environment is principally dependent bioremediation. Our goal was to isolate and characterize one 186 130 upon its chemical speciation. Thus, the aim is to either such organism from a field study area adjacent to a metals- 187 131 induce or maintain chemical conditions that result in metal contaminated environment and evaluate its potential for metal 188 132 species with reduced mobility. Depending on the ambient bioremediation. Here, we describe “Pelosinus lilae” UFO1, 189 133 redox conditions, many toxic metals and radionuclides can be isolated from the background or “pristine” area at the Oak 190 134 highly soluble, and thus mobile, in groundwater (Lovley, 2001). Ridge Field Research Center (ORFRC), Tennessee. The unique 191 135 Microorganisms are capable of altering chemical speciation phylogenetic and metal-transforming characteristics of “P. lilae” 192 136 via redox reactions, thereby influencing solubility, transport UFO1 reveal it is a novel species of a recently-described genus 193 137 properties, and bioavailability of metallic contaminants in designated Pelosinus. 194 138 subsurface environments. For example, bioreduction of highly 195 139 soluble Cr(VI) and U(VI) can result in conversion to insoluble 196 140 species [e.g., Cr(III) and U(IV)] that precipitate from solution MATERIALS AND METHODS 197 141 (Tabak et al., 2005). 198 142 Microbial Fe(III) reduction is an important environmental Enrichment and Isolation of Strain UFO1 199 143 process, and many Fe(III)-reducing bacteria have been found to Strict anaerobic techniques were used throughout this study 200 144 also reduce high-valence metal contaminants (Lloyd, 2003). In (Miller and Wolin, 1974; Balch and Wolfe, 1976). Sediment cores 201 145 addition, Fe(III)-reducing bacteria have been shown to utilize from the Field Research Center in Oak Ridge, TN, United States 202 146 humic acids and synthetic electron-shuttling moieties, such as were taken from background well 330, section 02-22 (FWB 203 147 anthraquinone-2,6-disulfonate (AQDS), as electron acceptors 330-02-22), at a depth of 0.61–1.12 m below the surface. The 204 148 (Lovley et al., 1996; Scott et al., 1998), which in turn can groundwater pH was 6.13. Samples were shipped and stored in 205 149 mediate the indirect reduction of Fe(III) and other metals (Lovley Mason jars under N2 and processed in an anaerobic glove bag 206 150 et al., 1998; Fredrickson et al., 2000; Nevin and Lovley, 2000). under N2-CO2-H2 (75:20:5). 207 151 The physiologic diversity of electron transport to ferruginous Enrichment cultures were initiated in 27 mL anaerobic 208 152 mineral substrates are distributed into distinct groups of Fe(III)- pressure tubes (Bellco Glass) containing 9 mL anaerobic 209 153 reducing microorganisms. One group consists of the respiratory freshwater medium (ATCC medium 2129) and ∼1 g FRC 210 154 Fe(III)-reducers, in which reduction occurs via an electron sediment.
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