Mechanisms of Mineral Substrate Acquisition in a Thermoacidophile

Abstract

The thermoacidophile Acidianus is widely distributed in Yellowstone National Park hot springs that span large gradients in pH (1.60 to 4.84), temperature (42 to 90°C), and mineralogical composition. To characterize the potential role of flexibility in mineral-dependent energy metabolism in contributing to the widespread ecological distribution of this organism, we characterized the spectrum of minerals capable of supporting metabolism and the mechanisms that it uses to access these minerals. The energy metabolism of Acidianus strain DS80 was supported by elemental sulfur (S⁰), a variety of iron (hydr)oxides, and arsenic sulfide. Strain DS80 reduced, oxidized, and disproportionated S⁰ Cells growing via S⁰ reduction and disproportionation did not require direct access to the mineral to reduce it, whereas cells growing via S⁰ oxidation did require direct access, observations that are attributable to the role of H₂S produced by S⁰ reduction/disproportionation in solubilizing and increasing the bioavailability of S⁰ Cells growing via iron (hydr)oxide reduction did not require access to the mineral, suggesting that the cells reduce Fe(III) that is being leached by the acidic growth medium. Cells growing via oxidation of arsenic sulfide with Fe(III) did not require access to the mineral to grow. The stoichiometry of reactants to products indicates that cells oxidize soluble As(III) released from oxidation of arsenic sulfide by aqueous Fe(III). Taken together, these observations underscore the importance of feedbacks between abiotic and biotic reactions in influencing the bioavailability of mineral substrates and defining ecological niches capable of supporting microbial metabolism.IMPORTANCE Mineral sources of electron donor and acceptor that support microbial metabolism are abundant in the natural environment. However, the spectrum of minerals capable of supporting a given microbial strain and the mechanisms that are used to access these minerals in support of microbial energy metabolism are often unknown, in particular among thermoacidophiles. Here, we show that the thermoacidophile Acidianus strain DS80 is adapted to use a variety of iron (hydro)oxide minerals, elemental sulfur, and arsenic sulfide to support growth. Cells rely on a complex interplay of abiologically and biologically catalyzed reactions that increase the solubility or bioavailability of minerals, thereby enabling their use in microbial metabolism.

Keywords: Yellowstone; acidophile; arsenic; elemental sulfur disproportionation; elemental sulfur oxidation; elemental sulfur reduction; ferric iron; iron reduction; realgar oxidation; thermophile.

FIG 1

The presence (black squares) or absence (white squares) of Acidianus sp. sor amplicons in DNA extracts from sediments collected from 73 hot springs in Yellowstone National Park plotted as a function of the pH and temperature of those springs.

FIG 2

Sulfide concentrations (A) and cell concentrations (B) in cultures of strain DS80 grown autotrophically with H₂ as electron donor and S⁰ as electron acceptor. S⁰ was provided in the bulk medium (control) or was sequestered in dialysis membranes (pore sizes of 12 to 14 kDa or 6 to 8 kDa) to prevent physical contact with the bulk mineral.

FIG 3

Fe(II) concentrations (A) and cell concentrations (B) in cultures of strain DS80 cultivated autotrophically with S⁰ as electron donor and Fe(III) (provided as ferric sulfate) as electron acceptor. S⁰ was provided in the bulk medium (control) or was sequestered in dialysis membranes (pore sizes of 12 to 14 kDa or 6 to 8 kDa) to prevent physical contact with the bulk mineral.

FIG 4

Sulfide concentrations (A), sulfate concentrations (B), cell concentrations (C), and available Gibbs free energy (ΔG) per mole of electrons transferred (D) in cultures of strain DS80 grown autotrophically with S⁰ provided as electron donor and acceptor (S⁰ disproportionation). S⁰ was provided in the bulk medium (control) or was sequestered in dialysis membranes (pore sizes of 12 to 14 kDa or 6 to 8 kDa) to prevent physical contact with the bulk mineral.

FIG 5

Fe(II) concentrations (A) and cell concentrations (B) in cultures of strain DS80 grown autotrophically with H₂ as electron donor and ferrihydrite as electron acceptor. Ferrihydrite was provided in the bulk medium (control) or was sequestered in dialysis membranes (pore sizes of 12 to 14 kDa or 6 to 8 kDa) to prevent physical contact with the bulk mineral. Note the scale difference in the y axis of panel B with respect to other growth conditions.

FIG 6

As(V) concentrations (A), Fe(II) concentrations (B), and cell concentrations (C) in cultures of strain DS80 grown autotrophically with realgar (α-As₄S₄) as electron donor and Fe(III) (provided as ferric sulfate) as electron acceptor. Realgar was provided in the bulk medium (control) or was sequestered in dialysis membranes (pore sizes of 12 to 14 kDa or 6 to 8 kDa) to prevent physical contact with the bulk mineral. Note the scale difference in the y axis of panel C with respect to other growth conditions.