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      Taxonomically-linked growth phenotypes during arsenic stress among arsenic resistant bacteria isolated from soils overlying the Centralia coal seam fire

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      1 , 2 , 3 , 1 , 4 , *

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          Abstract

          Arsenic (As), a toxic element, has impacted life since early Earth. Thus, microorganisms have evolved many As resistance and tolerance mechanisms to improve their survival outcomes given As exposure. We isolated As resistant bacteria from Centralia, PA, the site of an underground coal seam fire that has been burning since 1962. From a 57.4°C soil collected from a vent above the fire, we isolated 25 unique aerobic As resistant bacterial strains spanning seven genera. We examined their diversity, resistance gene content, transformation abilities, inhibitory concentrations, and growth phenotypes. Although As concentrations were low at the time of soil collection (2.58 ppm), isolates had high minimum inhibitory concentrations (MICs) of arsenate and arsenite (>300 mM and 20 mM respectively), and most isolates were capable of arsenate reduction. We screened isolates (PCR and sequencing) using 12 published primer sets for six As resistance genes (AsRGs). Genes encoding arsenate reductase ( arsC) and arsenite efflux pumps ( arsB, ACR3(2)) were present, and phylogenetic incongruence between 16S rRNA genes and AsRGs provided evidence for horizontal gene transfer. A detailed investigation of differences in isolate growth phenotypes across As concentrations (lag time to exponential growth, maximum growth rate, and maximum OD 590) showed a relationship with taxonomy, providing information that could help to predict an isolate’s performance given As exposure in situ. Our results suggest that microbiological management and remediation of environmental As could be informed by taxonomically-linked As tolerance, potential for resistance gene transferability, and the rare biosphere.

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          Most cited references53

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          Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species.

          Despite recent advances in commercially optimized identification systems, bacterial identification remains a challenging task in many routine microbiological laboratories, especially in situations where taxonomically novel isolates are involved. The 16S rRNA gene has been used extensively for this task when coupled with a well-curated database, such as EzTaxon, containing sequences of type strains of prokaryotic species with validly published names. Although the EzTaxon database has been widely used for routine identification of prokaryotic isolates, sequences from uncultured prokaryotes have not been considered. Here, the next generation database, named EzTaxon-e, is formally introduced. This new database covers not only species within the formal nomenclatural system but also phylotypes that may represent species in nature. In addition to an identification function based on Basic Local Alignment Search Tool (blast) searches and pairwise global sequence alignments, a new objective method of assessing the degree of completeness in sequencing is proposed. All sequences that are held in the EzTaxon-e database have been subjected to phylogenetic analysis and this has resulted in a complete hierarchical classification system. It is concluded that the EzTaxon-e database provides a useful taxonomic backbone for the identification of cultured and uncultured prokaryotes and offers a valuable means of communication among microbiologists who routinely encounter taxonomically novel isolates. The database and its analytical functions can be found at http://eztaxon-e.ezbiocloud.net/.
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            Information Theory and an Extension of the Maximumlikelihood Principle

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              Microbial arsenic: from geocycles to genes and enzymes.

              Arsenic compounds have been abundant at near toxic levels in the environment since the origin of life. In response, microbes have evolved mechanisms for arsenic resistance and enzymes that oxidize As(III) to As(V) or reduce As(V) to As(III). Formation and degradation of organoarsenicals, for example methylarsenic compounds, occur. There is a global arsenic geocycle, where microbial metabolism and mobilization (or immobilization) are important processes. Recent progress in studies of the ars operon (conferring resistance to As(III) and As(V)) in many bacterial types (and related systems in Archaea and yeast) and new understanding of arsenite oxidation and arsenate reduction by respiratory-chain-linked enzyme complexes has been substantial. The DNA sequencing and protein crystal structures have established the convergent evolution of three classes of arsenate reductases (that is classes of arsenate reductases are not of common evolutionary origin). Proposed reaction mechanisms in each case involve three cysteine thiols and S-As bond intermediates, so convergent evolution to similar mechanisms has taken place.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Methodology
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                25 January 2018
                2018
                : 13
                : 1
                Affiliations
                [1 ] Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America
                [2 ] Environmental and Integrative Toxicological Sciences Doctoral Program, Michigan State University, East Lansing, Michigan, United States of America
                [3 ] Lyman Briggs College, Michigan State University, East Lansing, Michigan, United States of America
                [4 ] Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, Michigan, United States of America
                University of Illinois at Urbana-Champaign, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-17-31362
                10.1371/journal.pone.0191893
                5785013
                29370270
                71557580-b33a-4aea-97db-1792b9ef0404
                © 2018 Dunivin et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 4, Tables: 1, Pages: 18
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100007709, Michigan State University;
                Award Recipient :
                The authors received no specific funding for this work. The project was supported by start-up funds from Michigan State University to AS. Michigan State University had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Chemistry
                Chemical Compounds
                Arsenates
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                Non-coding RNA
                Ribosomal RNA
                Biology and life sciences
                Biochemistry
                Ribosomes
                Ribosomal RNA
                Biology and life sciences
                Cell biology
                Cellular structures and organelles
                Ribosomes
                Ribosomal RNA
                Biology and Life Sciences
                Agriculture
                Agricultural Soil Science
                Ecology and Environmental Sciences
                Soil Science
                Agricultural Soil Science
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Engineering and Technology
                Energy and Power
                Fuels
                Fossil Fuels
                Coal
                Physical Sciences
                Materials Science
                Materials by Attribute
                Fuels
                Fossil Fuels
                Coal
                Physical Sciences
                Materials Science
                Organic Materials
                Coal
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Taxonomy
                Microbial Taxonomy
                Computer and Information Sciences
                Data Management
                Taxonomy
                Microbial Taxonomy
                Biology and Life Sciences
                Organisms
                Bacteria
                Enterobacter
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Enterobacter
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Enterobacter
                Custom metadata
                All sequences >200 bp were submitted to NCBI, and sequences can be accessed from GenBank with the following accession numbers: 16S rRNA KX825887- KX825911, arsC KY405022- KY405029, ACR3(2) KY405030- KY405032, and arsB KY405033- KY405040. Four arsC contigs were < 200 bp and are included in S3 Table.

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