TY - JOUR

T1 - Mixotrophic Iron-Oxidizing Thiomonas Isolates from an Acid Mine Drainage-Affected Creek

AU - Akob, Denise M.

AU - Hallenbeck, Michelle

AU - Beulig, Felix

AU - Fabisch, Maria

AU - Küsel, Kirsten

AU - Keffer, Jessica L.

AU - Woyke, Tanja

AU - Shapiro, Nicole

AU - Lapidus, Alla

AU - Klenk, Hans Peter

AU - Chan, Clara S.

N1 - Publisher Copyright: © 2020. All Rights Reserved. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/12

Y1 - 2020/12

N2 - Natural attenuation of heavy metals occurs via coupled microbial iron cycling and metal precipitation in creeks impacted by acid mine drainage (AMD). Here, we describe the isolation, characterization, and genomic sequencing of two iron-oxidizing bacteria (FeOB) species: Thiornonas ferrovorans FB-6 and Thiornonas rnetallidurans FB-Cd, isolated from slightly acidic (pH 6.3), Fe-rich, AMD-impacted creek sediments. These strains precipitated amorphous iron oxides, lepidocrocite, goethite, and magnetite or maghemite and grew at a pH optimum of 5.5. While Thiomonas spp. are known as mixotrophic sulfur oxidizers and As oxidizers, the FB strains oxidized Fe, which suggests they can efficiently remove Fe and other metals via coprecipitation. Previous evidence for Thiomonas sp. Fe oxidation is largely ambiguous, possibly because of difficulty demonstrating Fe oxidation in heterotrophic/mixotrophic organisms. Therefore, we also conducted a genomic analysis to identify genetic mechanisms of Fe oxidation, other metal transformations, and additional adaptations, comparing the two FB strain genomes with 12 other Thiornonas genomes. The FB strains fall within a relatively novel group of Thiomonas strains that includes another strain (b6) with solid evidence of Fe oxidation. Most Thiomonas isolates, including the FB strains, have the putative iron oxidation gene cyc2, but only the two FB strains possess the putative Fe oxidase genes rntoAB. The two FB strain genomes contain the highest numbers of strain-specific gene clusters, greatly increasing the known Thiornonas genetic potential. Our results revealed that the FB strains are two distinct novel species of Thiomonas with the genetic potential for bioremediation of AMD via iron oxidation.IMPORTANCE As AMD moves through the environment, it impacts aquatic ecosystems, but at the same time, these ecosystems can naturally attenuate contaminated waters via acid neutralization and catalyzing metal precipitation. This is the case in the former Ronneburg uranium-mining district, where AMD impacts creek sediments. We isolated and characterized two iron-oxidizing Thiomonas species that are mildly acidophilic to neutrophilic and that have two genetic pathways for iron oxidation. These Thiomonas species are well positioned to naturally attenuate AMD as it discharges across the landscape.

AB - Natural attenuation of heavy metals occurs via coupled microbial iron cycling and metal precipitation in creeks impacted by acid mine drainage (AMD). Here, we describe the isolation, characterization, and genomic sequencing of two iron-oxidizing bacteria (FeOB) species: Thiornonas ferrovorans FB-6 and Thiornonas rnetallidurans FB-Cd, isolated from slightly acidic (pH 6.3), Fe-rich, AMD-impacted creek sediments. These strains precipitated amorphous iron oxides, lepidocrocite, goethite, and magnetite or maghemite and grew at a pH optimum of 5.5. While Thiomonas spp. are known as mixotrophic sulfur oxidizers and As oxidizers, the FB strains oxidized Fe, which suggests they can efficiently remove Fe and other metals via coprecipitation. Previous evidence for Thiomonas sp. Fe oxidation is largely ambiguous, possibly because of difficulty demonstrating Fe oxidation in heterotrophic/mixotrophic organisms. Therefore, we also conducted a genomic analysis to identify genetic mechanisms of Fe oxidation, other metal transformations, and additional adaptations, comparing the two FB strain genomes with 12 other Thiornonas genomes. The FB strains fall within a relatively novel group of Thiomonas strains that includes another strain (b6) with solid evidence of Fe oxidation. Most Thiomonas isolates, including the FB strains, have the putative iron oxidation gene cyc2, but only the two FB strains possess the putative Fe oxidase genes rntoAB. The two FB strain genomes contain the highest numbers of strain-specific gene clusters, greatly increasing the known Thiornonas genetic potential. Our results revealed that the FB strains are two distinct novel species of Thiomonas with the genetic potential for bioremediation of AMD via iron oxidation.IMPORTANCE As AMD moves through the environment, it impacts aquatic ecosystems, but at the same time, these ecosystems can naturally attenuate contaminated waters via acid neutralization and catalyzing metal precipitation. This is the case in the former Ronneburg uranium-mining district, where AMD impacts creek sediments. We isolated and characterized two iron-oxidizing Thiomonas species that are mildly acidophilic to neutrophilic and that have two genetic pathways for iron oxidation. These Thiomonas species are well positioned to naturally attenuate AMD as it discharges across the landscape.

KW - pangenome

KW - iron oxidation

KW - heavy metals

KW - Thiomonas

KW - acid mine drainage

KW - cyc2

KW - Thiomonas

KW - acid mine drainage

KW - cyc2

KW - heavy metals

KW - iron oxidation

KW - pangenome

KW - Burkholderiales/metabolism

KW - Oxidation-Reduction

KW - Waste Water/microbiology

KW - Mining

KW - Rivers/microbiology

KW - Iron/metabolism

KW - Germany

KW - OXIDATION

KW - FE(II)-OXIDIZING BACTERIA

KW - MECHANISMS

KW - ANAEROBIC BIOOXIDATION

KW - SP NOV.

KW - IMMOBILIZATION

KW - ARSENITE

KW - RESIDUAL CONTAMINATION

KW - CARNOULES

KW - THIOBACILLUS-DELICATUS

UR - http://www.scopus.com/inward/record.url?scp=85096885221&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/54c92a9c-f18a-34e2-94a6-4b89d6924c64/

U2 - 10.1128/AEM.01424-20

DO - 10.1128/AEM.01424-20

M3 - Article

C2 - 33008825

AN - SCOPUS:85096885221

VL - 86

SP - 1

EP - 18

JO - Applied Microbiology

JF - Applied Microbiology

SN - 0099-2240

IS - 24

M1 - ARTN e01424-20

ER -