Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes

Acidic pit lakes are abandoned open pit mines filled with acid mine drainage (AMD)—highly acidic, metalliferous waters that pose a severe threat to the environment and are rarely properly remediated.<b> </b>Here, we investigated two meromictic, oligotrophic acidic mine pit lakes in the I...

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Main Authors: Charlotte M. van der Graaf, Javier Sánchez-España, Iñaki Yusta, Andrey Ilin, Sudarshan A. Shetty, Nicole J. Bale, Laura Villanueva, Alfons J. M. Stams, Irene Sánchez-Andrea
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/8/9/1275
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author Charlotte M. van der Graaf
Javier Sánchez-España
Iñaki Yusta
Andrey Ilin
Sudarshan A. Shetty
Nicole J. Bale
Laura Villanueva
Alfons J. M. Stams
Irene Sánchez-Andrea
author_facet Charlotte M. van der Graaf
Javier Sánchez-España
Iñaki Yusta
Andrey Ilin
Sudarshan A. Shetty
Nicole J. Bale
Laura Villanueva
Alfons J. M. Stams
Irene Sánchez-Andrea
author_sort Charlotte M. van der Graaf
collection DOAJ
description Acidic pit lakes are abandoned open pit mines filled with acid mine drainage (AMD)—highly acidic, metalliferous waters that pose a severe threat to the environment and are rarely properly remediated.<b> </b>Here, we investigated two meromictic, oligotrophic acidic mine pit lakes in the Iberian Pyrite Belt (IPB), Filón Centro (Tharsis) (FC) and La Zarza (LZ). We observed a natural attenuation of acidity and toxic metal concentrations towards the lake bottom, which was more pronounced in FC. The detection of Cu and Zn sulfides in the monimolimnion of FC suggests precipitation of dissolved metals as metal sulfides, pointing to biogenic sulfide formation. This was supported by microbial diversity analysis via 16S rRNA gene amplicon sequencing of samples from the water column, which showed the presence of sulfidogenic microbial taxa in FC and LZ. In the monimolimnion of FC, sequences affiliated with the putative sulfate-reducing genus <i>Desulfomonile</i><i> </i>were dominant (58%), whereas in the more acidic and metal-enriched LZ, elemental sulfur-reducing <i>Acidianus</i><i> </i>and <i>Thermoplasma</i><i> spp.</i>, and disproportionating <i>Desulfocapsa</i><i> spp</i>. were more abundant. Furthermore, the detection of reads classified as methanogens and <i>Desulfosporosinus</i><i> spp.</i>, although at low relative abundance, represents one of the lowest pH values (2.9 in LZ) at which these taxa have been reported, to our knowledge. Analysis of potential biomarker lipids provided evidence that high levels of phosphocholine lipids with mixed acyl/ether glycerol core structures were associated with <i>Desulfomonile</i>,<i> </i>while ceramide lipids were characteristic of <i>Microbacter</i><i> </i>in these environments. We propose that FC and LZ function as natural bioremediation reactors where metal sulfide precipitation is mediated by biosulfidogenesis starting from elemental sulfur reduction and disproportionation at an early stage (LZ), followed by sulfate reduction at a later stage (FC).
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spelling doaj.art-deaf4d65ac944383bec1606ddfc1a4aa2023-11-20T10:55:16ZengMDPI AGMicroorganisms2076-26072020-08-0189127510.3390/microorganisms8091275Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit LakesCharlotte M. van der Graaf0Javier Sánchez-España1Iñaki Yusta2Andrey Ilin3Sudarshan A. Shetty4Nicole J. Bale5Laura Villanueva6Alfons J. M. Stams7Irene Sánchez-Andrea8Laboratory of Microbiology, Wageningen University, Stippeneng 4, 6708 WE Wageningen, The NetherlandsGeochemistry and Sustainable Mining Unit, Department of Geological Resources, Spanish Geological Survey (IGME), Calera 1, Tres Cantos, 28760 Madrid, SpainDepartment of Mineralogy and Petrology, University of the Basque Country (UPV/EHU), Apdo. 644, 48080 Bilbao, SpainDepartment of Mineralogy and Petrology, University of the Basque Country (UPV/EHU), Apdo. 644, 48080 Bilbao, SpainLaboratory of Microbiology, Wageningen University, Stippeneng 4, 6708 WE Wageningen, The NetherlandsNIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, Landsdiep 4, 1797 SZ ‘t Horntje, The NetherlandsNIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, and Utrecht University, Landsdiep 4, 1797 SZ ‘t Horntje, The NetherlandsLaboratory of Microbiology, Wageningen University, Stippeneng 4, 6708 WE Wageningen, The NetherlandsLaboratory of Microbiology, Wageningen University, Stippeneng 4, 6708 WE Wageningen, The NetherlandsAcidic pit lakes are abandoned open pit mines filled with acid mine drainage (AMD)—highly acidic, metalliferous waters that pose a severe threat to the environment and are rarely properly remediated.<b> </b>Here, we investigated two meromictic, oligotrophic acidic mine pit lakes in the Iberian Pyrite Belt (IPB), Filón Centro (Tharsis) (FC) and La Zarza (LZ). We observed a natural attenuation of acidity and toxic metal concentrations towards the lake bottom, which was more pronounced in FC. The detection of Cu and Zn sulfides in the monimolimnion of FC suggests precipitation of dissolved metals as metal sulfides, pointing to biogenic sulfide formation. This was supported by microbial diversity analysis via 16S rRNA gene amplicon sequencing of samples from the water column, which showed the presence of sulfidogenic microbial taxa in FC and LZ. In the monimolimnion of FC, sequences affiliated with the putative sulfate-reducing genus <i>Desulfomonile</i><i> </i>were dominant (58%), whereas in the more acidic and metal-enriched LZ, elemental sulfur-reducing <i>Acidianus</i><i> </i>and <i>Thermoplasma</i><i> spp.</i>, and disproportionating <i>Desulfocapsa</i><i> spp</i>. were more abundant. Furthermore, the detection of reads classified as methanogens and <i>Desulfosporosinus</i><i> spp.</i>, although at low relative abundance, represents one of the lowest pH values (2.9 in LZ) at which these taxa have been reported, to our knowledge. Analysis of potential biomarker lipids provided evidence that high levels of phosphocholine lipids with mixed acyl/ether glycerol core structures were associated with <i>Desulfomonile</i>,<i> </i>while ceramide lipids were characteristic of <i>Microbacter</i><i> </i>in these environments. We propose that FC and LZ function as natural bioremediation reactors where metal sulfide precipitation is mediated by biosulfidogenesis starting from elemental sulfur reduction and disproportionation at an early stage (LZ), followed by sulfate reduction at a later stage (FC).https://www.mdpi.com/2076-2607/8/9/1275acidophilessulfate reductionsulfur reductionsulfur disproportionationbiosulfidogenesisbioremediation
spellingShingle Charlotte M. van der Graaf
Javier Sánchez-España
Iñaki Yusta
Andrey Ilin
Sudarshan A. Shetty
Nicole J. Bale
Laura Villanueva
Alfons J. M. Stams
Irene Sánchez-Andrea
Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes
Microorganisms
acidophiles
sulfate reduction
sulfur reduction
sulfur disproportionation
biosulfidogenesis
bioremediation
title Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes
title_full Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes
title_fullStr Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes
title_full_unstemmed Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes
title_short Biosulfidogenesis Mediates Natural Attenuation in Acidic Mine Pit Lakes
title_sort biosulfidogenesis mediates natural attenuation in acidic mine pit lakes
topic acidophiles
sulfate reduction
sulfur reduction
sulfur disproportionation
biosulfidogenesis
bioremediation
url https://www.mdpi.com/2076-2607/8/9/1275
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