Evidence for fungi and gold redox interaction under Earth surface conditions

Abstract

Microbial contribution to gold biogeochemical cycling has been proposed. However, studies have focused primarily on the influence of prokaryotes on gold reduction and precipitation through a detoxification-oriented mechanism. Here we show, fungi, a major driver of mineral bioweathering, can initiate gold oxidation under Earth surface conditions, which is of significance for dissolved gold species formation and distribution. Presence of the gold-oxidizing fungus TA_pink1, an isolate of Fusarium oxysporum, suggests fungi have the potential to substantially impact gold biogeochemical cycling. Our data further reveal that indigenous fungal diversity positively correlates with in situ gold concentrations. Hypocreales, the order of the gold-oxidizing fungus, show the highest centrality in the fungal microbiome of the auriferous environment. Therefore, we argue that the redox interaction between fungi and gold is critical and should be considered in gold biogeochemical cycling.

Fig. 1

Soil geochemical parameters of the gold anomaly and the adjacent reference area. a–i represent the values of total carbon, total nitrogen, soil pH, electrical conductivity, water content, the concentrations of gold, iron, calcium, and sulfur. The bars H, N, and A in each panel represent the data of the hotspots, the non-hotspots, and all spots of the gold anomaly, respectively. The significance of the differences between two sets of data was determined by an unpaired t-test (GraphPad Prism Version 7). The P value for gold content was based on a one-tailed t-test calculation. P < 0.05 was considered statistically significant. The error bar indicates the standard deviation

Fig. 2

Microbial gold oxidation potential and geochemical modeling in soil microcosms. a–c Time-dependence between Au(III) concentration and pH in different microcosms expressed as means of triplicates ± standard deviation. a Gold oxidation in fungal microcosms GA6F+cs and RA6F+cs, with ① and ② marking the first and second linear phases of gold oxidation in microcosm GA6F+cs. b Bacterial microcosms GA8B+cyc and RA8B+cyc. c Sterilized microcosms GA6I and RA6I. d, e Geochemical models showing predominant Au speciation as a function of pH-Eh at 25 °C. The systems contain initial Au⁺ activity of 10⁻⁶ to 10⁻¹², and HCO₃^- activity of 0.01 (d) or S₂O₃^2- activity of 0.01 (e). The carbon and sulfur species are reacted with the axis species, and the dashed gray lines show the boundary of predominant carbon and sulfur species over pH-Eh conditions. Predominant Au speciation at 1 part per trillion (ppt) (solid red line), 1 part per billion (ppb) (dashed orange line), and 1 part per million (ppm) (dashed yellow line) is indicated. Blue arrows show the direction of gold mineralization

Fig. 3

Gold-oxidizing capacity of TA_pink1. a TA_pink1 was inoculated at the center of PYG agar plates supplemented with 400 μM colloidal gold. After 14 days of incubation at 10 °C in the dark, a gold-dissolving halo appeared around the central colony, dividing the agar into three zones: center, oxidized zone, and undisturbed zone. Scale bar, 1 cm. b Quantification of gold intensity in different zones of the PYG agar by LA-ICP-MS. The horizontal axis represents the gold signal in counts s⁻¹. Error bars represent standard deviation, *P < 0.001. c Expanded gold profile from XPS analysis. The inset shows profiles of major elements, including signals from O 1s (531.0 eV), C 1s (285.1 eV), N 1s (399.5 eV), and Au 4f (84.0 eV). High-resolution scans of C 1s (d–f) and Au 4f spectra (g–i) from different zones. Gray dots represent the intensity of the spectra in counts per second (cps)

Fig. 4

Interaction between TA_pink1 and colloidal gold in liquid media. a Cyclic voltammograms of TA_pink1 after 0 and 17 h of incubation in the presence and absence of colloidal gold. Control, TA_pink1 incubated without colloidal gold. b Scanning electron micrographs of colloidal gold (CG) with the fungal hyphae (FH) of TA_pink1in liquid PYG medium after 14 days of incubation at 10 °C. Scale bar, 5 µm. c Detailed view of nanometer gold particles and surrounding materials (yellow arrows) over the surface of fungal hyphae. Scale bar, 5 µm. The inset shows an EDS profile of the major components of the assemblage

Fig. 5

Hyphal extension of TA_pink1. (a) sucrose and (b) lignin as the sole carbon source. Error bars denote the standard deviation of the mean of triplicate measurements and are only shown when greater than the symbol dimension

Fig. 6

Co-occurring ecological networks of fungal OTUs (order level) according to the random matrix theory. Each node represents an OTU. The connectivity between two OTUs is indicated by an edge. Blue and red edges represent positive and negative correlations, respectively. The colors of the nodes denote different phyla. The greedy modularity optimization method was used to form each of the three ecological network modules in the gold anomaly (a–c) and the reference (d–f) from fungal communities. The size of each circle indicates the degree of Stress Centrality c_S(x) to each OTU in the gold anomaly and the reference area. The Stress Centrality index is used to describe the approximate amount of stress a node x has to sustain in the network by counting the number of short paths that contain node x. Thus, a node is more central when more short paths run through it. The node at the six o’clock position of each module has the most connections to other nodes. The degree of connection decreases counterclockwise. Detailed taxonomic annotations and the network nodes’ centrality indexes for each OTU are shown in Supplementary Data 2–4

Fig. 7

The conceptual model for mycological gold redox transformation under Earth surface conditions. Superoxides from fungal hyphae oxidatively dissolve colloidal gold to gold ions with likely assistance of protons. Gold ions then complex with the intracellularly produced ligand. Colloidal gold nanoparticles may be regenerated from the interaction between gold complexes and reduced organic carbon species. Dashed arrows indicate superoxides and ligands are produced intracellularly