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. 2022 Feb 9:12:819804.
doi: 10.3389/fmicb.2021.819804. eCollection 2021.

Correlation Between Fe/S/As Speciation Transformation and Depth Distribution of Acidithiobacillus ferrooxidans and Acidiphilium acidophilum in Simulated Acidic Water Column

Yu-Hang Zhou  1 , Can Wang  1 , Hong-Chang Liu  1 , Zhen Xue  1 , Zhen-Yuan Nie  1 , Yue Liu  1 , Jiao-Li Wan  1 , Yu Yang  1 , Wen-Sheng Shu  2 , Jin-Lan Xia  1
Affiliations

Correlation Between Fe/S/As Speciation Transformation and Depth Distribution of Acidithiobacillus ferrooxidans and Acidiphilium acidophilum in Simulated Acidic Water Column

Yu-Hang Zhou et al. Front Microbiol. .

Abstract

It is well known that speciation transformations of As(III) vs. As(V) in acid mine drainage (AMD) are mainly driven by microbially mediated redox reactions of Fe and S. However, these processes are rarely investigated. In this study, columns containing mine water were inoculated with two typical acidophilic Fe/S-oxidizing/reducing bacteria [the chemoautotrophic Acidithiobacillus (At.) ferrooxidans and the heterotrophic Acidiphilium (Aph.) acidophilum], and three typical energy substrates (Fe2+, S0, and glucose) and two concentrations of As(III) (2.0 and 4.5 mM) were added. The correlation between Fe/S/As speciation transformation and bacterial depth distribution at three different depths, i.e., 15, 55, and 105 cm from the top of the columns, was comparatively investigated. The results show that the cell growth at the top and in the middle of the columns was much more significantly inhibited by the additions of As(III) than at the bottom, where the cell growth was promoted even on days 24-44. At. ferrooxidans dominated over Aph. acidophilum in most samples collected from the three depths, but the elevated proportions of Aph. acidophilum were observed in the top and bottom column samples when 4.5 mM As(III) was added. Fe2+ bio-oxidation and Fe3+ reduction coupled to As(III) oxidation occurred for all three column depths. At the column top surfaces, jarosites were formed, and the addition of As(III) could lead to the formation of the amorphous FeAsO4⋅2H2O. Furthermore, the higher As(III) concentration could inhibit Fe2+ bio-oxidation and the formation of FeAsO4⋅2H2O and jarosites. S oxidation coupled to Fe3+ reduction occurred at the bottom of the columns, with the formations of FeAsO4⋅2H2O precipitate and S intermediates. The formed FeAsO4⋅2H2O and jarosites at the top and bottom of the columns could adsorb to and coprecipitate with As(III) and As(V), resulting in the transfer of As from solution to solid phases, thus further affecting As speciation transformation. The distribution difference of Fe/S energy substrates could apparently affect Fe/S/As speciation transformation and bacterial depth distribution between the top and bottom of the water columns. These findings are valuable for elucidating As fate and toxicity mediated by microbially driven Fe/S redox in AMD environments.

Keywords: Acidiphilium acidophilum; Acidithiobacillus ferrooxidans; Fe/S redox reactions; Fe/S/As speciation transformation; acid mine drainage.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Cell density (A–C) and bacterial composition (D–F) for the top (A,D), middle (B,E), and bottom (C,F) of the water columns without (Col_0) and with additions of 2.0 mM (Col_2.0) and 4.5 mM (Col_4.5) As(III). The initial cell density of At. ferrooxidans and Aph. acidophilum was the same, i.e., 2.5 × 107 cells/ml.
FIGURE 2
FIGURE 2
The curves of pH (A–C), [Fe3+] (D–F), and [Fe2+] (G–I) in the solutions at the top (A,D,G,J), middle (B,E,H,K), and bottom (C,F,I,L) of the water columns during cultivation without (Col_0) and with additions of 2.0 mM (Col_2.0) and 4.5 mM (Col_4.5) As(III), and the curves of [As(III)] and [As(V)] (J–L) with additions of 2.0 and 4.5 mM As(III). Error bars represent SD, n = 3.
FIGURE 3
FIGURE 3
FT-IR spectra (A) and XPS spectra of the surface As (B,C), S (D–F), and Fe (G–I) for the surface suspended matter at 24/105, 105, and 120 days of the water columns without (Col_0) and with additions of 2.0 mM (Col_2.0) and 4.5 mM (Col_4.5) As(III), respectively.
FIGURE 4
FIGURE 4
Normalized Fe L-edge XANES spectra for the bottom residues during cultivation without (A) and with additions of 2.0 mM (B) and 4.5 mM (C) As(III), where the green and blue bands represent Fe(II) and Fe(III) species, respectively.
FIGURE 5
FIGURE 5
S K-edge XANES spectra for the reference samples (A), and the bottom residues during cultivation without (B) and with additions of 2.0 mM (C) and 4.5 mM (D) As(III).
FIGURE 6
FIGURE 6
XPS spectra for the surface S of the bottom residues during cultivation without (A–E) and with additions of 2.0 mM (F–J) and 4.5 mM (K–O) As(III) on days 8 (A,F,K), 40 (B,G,L), 74 (C,H,M), 110 (D,I,N), and 140 (E,J,O).
FIGURE 7
FIGURE 7
XPS spectra for the surface As of bottom residues during cultivation with additions of 2.0 mM (A–E) and 4.5 mM (F–J) As(III) on days 8, 40, 74, 110, and 140.
FIGURE 8
FIGURE 8
The diagram of the correlation between Fe/S/As speciation transformation and bacterial (At. ferrooxidans and Aph. acidophilum) depth distribution under different depths of the acidic water column. Dashed arrows show the migration of the dissolved ions, and solid arrows show the Fe/S/As redox reactions.
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