Micro-colonization of arsenic-resistant Staphylococcus sp. As-3 on arsenopyrite (FeAsS) drives arsenic mobilization under anoxic sub-surface mimicking conditions

Jagat Rathod, Jiin-Shuh Jean, Wei-Teh Jiang, I-Hsiu Huang, Bernard Haochih Liu, Yao Chang Lee

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Abstract

We investigated the subsurface biomatrix of the most abundant As-mineral, arsenopyrite (FeAsS), and meticulously studied a potential biogenic arsenic mobilization phenomenon. An arsenic-resistant [up to 7.5 mM As(III) and 200 mM As(V)] and arsenate-reducing bacterial strain (Staphylococcus sp. As-3) was isolated from a sediment core sample taken from the Budai borehole, on the southwestern coast of Taiwan. Isolate As-3 could reduce 5 mM As(V) to 3.04 mM in 96 h, generating 1.6 mM As(III) under anoxic conditions. Isolate As-3, which adsorbed As(V) up to 19.02 mg g −1 (cdw) and As(III) up to 0.46 mg g −1 (cdw), demonstrated effective As-bioaccumulating ability, as corroborated by a TEM-EDS analysis. Under anaerobic batch conditions, isolate As-3 micro-colonies could grow on as well as interact with arsenopyrite (FeAsS), mobilizing arsenic into soluble phase as As(III) and As(V). Using synchrotron radiation-based FTIR micro-spectroscopy, various functional group signatures and critical chemical bonds enabling a direct interaction with arsenopyrite were underpinned, such as a potential P-OFe bond involved in facilitating bacteria-mineral interaction. Using atomic force microscopy, we analyzed the scattered bacterial cell arrangement and structure and measured various biomechanical properties of micro-colonized Staphylococcus sp. As-3 cells on arsenopyrite. We suggest that the release of organic acids from As-3 drives soluble arsenic release in the aqueous phase under anoxic conditions through oxidative dissolution. Furthermore, arsC-encoding putative cytoplasmic arsenic reductase sequencing and transcript characterization indicated that arsC plays a possible role in the reduction of moderately soluble As(V) to highly soluble toxic As(III) under anoxic conditions. Thus, we suggest that firmicutes such as Staphylococcus sp. As-3 may play an important role in microbially-mediated arsenic mobilization, leading to arsenic release in the sub-surface niche.

Original languageEnglish
Pages (from-to)527-539
Number of pages13
JournalScience of the Total Environment
Volume669
DOIs
Publication statusPublished - 2019 Jun 15

Fingerprint

arsenopyrite
Arsenic
mobilization
arsenic
colonization
anoxic conditions
Minerals
Core samples
atomic force microscopy
Poisons
Chemical bonds
Organic acids
arsenate
mineral
Synchrotron radiation
Boreholes
organic acid
Functional groups
functional group
sediment core

All Science Journal Classification (ASJC) codes

  • Environmental Engineering
  • Environmental Chemistry
  • Waste Management and Disposal
  • Pollution

Cite this

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title = "Micro-colonization of arsenic-resistant Staphylococcus sp. As-3 on arsenopyrite (FeAsS) drives arsenic mobilization under anoxic sub-surface mimicking conditions",
abstract = "We investigated the subsurface biomatrix of the most abundant As-mineral, arsenopyrite (FeAsS), and meticulously studied a potential biogenic arsenic mobilization phenomenon. An arsenic-resistant [up to 7.5 mM As(III) and 200 mM As(V)] and arsenate-reducing bacterial strain (Staphylococcus sp. As-3) was isolated from a sediment core sample taken from the Budai borehole, on the southwestern coast of Taiwan. Isolate As-3 could reduce 5 mM As(V) to 3.04 mM in 96 h, generating 1.6 mM As(III) under anoxic conditions. Isolate As-3, which adsorbed As(V) up to 19.02 mg g −1 (cdw) and As(III) up to 0.46 mg g −1 (cdw), demonstrated effective As-bioaccumulating ability, as corroborated by a TEM-EDS analysis. Under anaerobic batch conditions, isolate As-3 micro-colonies could grow on as well as interact with arsenopyrite (FeAsS), mobilizing arsenic into soluble phase as As(III) and As(V). Using synchrotron radiation-based FTIR micro-spectroscopy, various functional group signatures and critical chemical bonds enabling a direct interaction with arsenopyrite were underpinned, such as a potential P-OFe bond involved in facilitating bacteria-mineral interaction. Using atomic force microscopy, we analyzed the scattered bacterial cell arrangement and structure and measured various biomechanical properties of micro-colonized Staphylococcus sp. As-3 cells on arsenopyrite. We suggest that the release of organic acids from As-3 drives soluble arsenic release in the aqueous phase under anoxic conditions through oxidative dissolution. Furthermore, arsC-encoding putative cytoplasmic arsenic reductase sequencing and transcript characterization indicated that arsC plays a possible role in the reduction of moderately soluble As(V) to highly soluble toxic As(III) under anoxic conditions. Thus, we suggest that firmicutes such as Staphylococcus sp. As-3 may play an important role in microbially-mediated arsenic mobilization, leading to arsenic release in the sub-surface niche.",
author = "Jagat Rathod and Jiin-Shuh Jean and Wei-Teh Jiang and I-Hsiu Huang and Liu, {Bernard Haochih} and Lee, {Yao Chang}",
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T1 - Micro-colonization of arsenic-resistant Staphylococcus sp. As-3 on arsenopyrite (FeAsS) drives arsenic mobilization under anoxic sub-surface mimicking conditions

AU - Rathod, Jagat

AU - Jean, Jiin-Shuh

AU - Jiang, Wei-Teh

AU - Huang, I-Hsiu

AU - Liu, Bernard Haochih

AU - Lee, Yao Chang

PY - 2019/6/15

Y1 - 2019/6/15

N2 - We investigated the subsurface biomatrix of the most abundant As-mineral, arsenopyrite (FeAsS), and meticulously studied a potential biogenic arsenic mobilization phenomenon. An arsenic-resistant [up to 7.5 mM As(III) and 200 mM As(V)] and arsenate-reducing bacterial strain (Staphylococcus sp. As-3) was isolated from a sediment core sample taken from the Budai borehole, on the southwestern coast of Taiwan. Isolate As-3 could reduce 5 mM As(V) to 3.04 mM in 96 h, generating 1.6 mM As(III) under anoxic conditions. Isolate As-3, which adsorbed As(V) up to 19.02 mg g −1 (cdw) and As(III) up to 0.46 mg g −1 (cdw), demonstrated effective As-bioaccumulating ability, as corroborated by a TEM-EDS analysis. Under anaerobic batch conditions, isolate As-3 micro-colonies could grow on as well as interact with arsenopyrite (FeAsS), mobilizing arsenic into soluble phase as As(III) and As(V). Using synchrotron radiation-based FTIR micro-spectroscopy, various functional group signatures and critical chemical bonds enabling a direct interaction with arsenopyrite were underpinned, such as a potential P-OFe bond involved in facilitating bacteria-mineral interaction. Using atomic force microscopy, we analyzed the scattered bacterial cell arrangement and structure and measured various biomechanical properties of micro-colonized Staphylococcus sp. As-3 cells on arsenopyrite. We suggest that the release of organic acids from As-3 drives soluble arsenic release in the aqueous phase under anoxic conditions through oxidative dissolution. Furthermore, arsC-encoding putative cytoplasmic arsenic reductase sequencing and transcript characterization indicated that arsC plays a possible role in the reduction of moderately soluble As(V) to highly soluble toxic As(III) under anoxic conditions. Thus, we suggest that firmicutes such as Staphylococcus sp. As-3 may play an important role in microbially-mediated arsenic mobilization, leading to arsenic release in the sub-surface niche.

AB - We investigated the subsurface biomatrix of the most abundant As-mineral, arsenopyrite (FeAsS), and meticulously studied a potential biogenic arsenic mobilization phenomenon. An arsenic-resistant [up to 7.5 mM As(III) and 200 mM As(V)] and arsenate-reducing bacterial strain (Staphylococcus sp. As-3) was isolated from a sediment core sample taken from the Budai borehole, on the southwestern coast of Taiwan. Isolate As-3 could reduce 5 mM As(V) to 3.04 mM in 96 h, generating 1.6 mM As(III) under anoxic conditions. Isolate As-3, which adsorbed As(V) up to 19.02 mg g −1 (cdw) and As(III) up to 0.46 mg g −1 (cdw), demonstrated effective As-bioaccumulating ability, as corroborated by a TEM-EDS analysis. Under anaerobic batch conditions, isolate As-3 micro-colonies could grow on as well as interact with arsenopyrite (FeAsS), mobilizing arsenic into soluble phase as As(III) and As(V). Using synchrotron radiation-based FTIR micro-spectroscopy, various functional group signatures and critical chemical bonds enabling a direct interaction with arsenopyrite were underpinned, such as a potential P-OFe bond involved in facilitating bacteria-mineral interaction. Using atomic force microscopy, we analyzed the scattered bacterial cell arrangement and structure and measured various biomechanical properties of micro-colonized Staphylococcus sp. As-3 cells on arsenopyrite. We suggest that the release of organic acids from As-3 drives soluble arsenic release in the aqueous phase under anoxic conditions through oxidative dissolution. Furthermore, arsC-encoding putative cytoplasmic arsenic reductase sequencing and transcript characterization indicated that arsC plays a possible role in the reduction of moderately soluble As(V) to highly soluble toxic As(III) under anoxic conditions. Thus, we suggest that firmicutes such as Staphylococcus sp. As-3 may play an important role in microbially-mediated arsenic mobilization, leading to arsenic release in the sub-surface niche.

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