Persistent Bacterial and Fungal Community Shifts Exhibited in Selenium-Contaminated Reclaimed Mine Soils

Abstract

Mining and other industrial activities worldwide have resulted in Se-enriched surface soils, which pose risks to human and environmental health. Although not well studied, microbial activity can alter Se bioavailability and distribution, even in oxic environments. We used high-throughput sequencing to profile bacterial and fungal communities inhabiting mine soils in southeastern Idaho, comparing mined and unmined locations within two reclaimed phosphate mine areas containing various Se concentrations. The goal was to determine whether microbial communities differed in (i) different mines, (ii) mined areas compared to unmined areas, and (iii) various soil Se concentrations. Though reclamation occurred 20 to 30 years ago, microbial community structures in mined soils were significantly altered compared to unmined soils, suggesting persistent mining-related impacts on soil processes. Additionally, operational taxonomic unit with a 97% sequence similarity cutoff (OTU_0.03) richness and diversity were significantly diminished with increasing Se, though not with other geochemical parameters, suggesting that Se contamination shapes communities in favor of Se-tolerant microorganisms. Two bacterial phyla, Actinobacteria and Gemmatimonadetes, were enriched in high-Se soils, while for fungi, Ascomycota dominated all soils regardless of Se concentration. Combining diversity analyses and taxonomic patterns enables us to move toward connecting physiological function of microbial groups to Se biogeochemical cycling in oxic soil environments.IMPORTANCE Selenium contamination in natural environments is of great concern globally, and microbial processes are known to mediate Se transformations. Such transformations alter Se mobility, bioavailability, and toxicity, which can amplify or mitigate Se pollution. To date, nearly all studies investigating Se-microbe interactions have used culture-based approaches with anaerobic bacteria despite growing knowledge that (i) aerobic Se transformations can occur, (ii) such transformations can be mediated by microorganisms other than bacteria, and (iii) microbial community dynamics, rather than individual organismal activities, are important for metal(loid) cycling in natural environments. We examined bacterial and fungal communities in Se-contaminated reclaimed mine soils and found significant declines in diversity at high Se concentrations. Additionally, we identified specific taxonomic groups that tolerate excess Se and may be useful for bioremediation purposes. These patterns were similar across mines of different ages, suggesting that microbial community impacts may persist long after physicochemical parameters indicate complete site recovery.

Keywords: metalloids; metals; microbial ecology; microbiome; pollution.

FIG 1

Linear regressions (black lines) of three diversity measures (inverse Simpson diversity index, OTU richness, and Shannon diversity index), as a function of soil [Se] for bacteria (A) and fungi (B) in the Champ Mine (dark blue, closed symbols), Champ references (dark blue, open symbols), Mountain Fuel Mine (yellow, closed symbols), and Mountain Fuel reference (yellow, open symbols). Each data point represents an individual sample taken in either 2015 (circles) or 2016 (triangles). Gray shading is the 95% confidence interval calculated for the linear regressions. Pearson correlation coefficients (R²_adj) and P values are listed in the top right or bottom left of each panel. Regressions were considered statistically significant with P values of <0.05.

FIG 2

Principal-coordinate analysis of bacterial (A) and fungal (B) β-diversity in Champ Mine, Mountain (Mtn) Fuel Mine, Champ reference, and Mountain Fuel reference sites. Axis 1 represents 17% and 11% of the ordination variation for bacteria and fungi, respectively. Axis 2 explains 10% and 6% of the variation for bacteria and fungi, respectively. Operational taxonomic unit (OTU) abundances were Hellinger transformed prior to dissimilarity calculation. Black lines indicate environmental factors with significant correlations (P_adj < 0.05) to the bacterial and fungal OTU ordinations. Lines are scaled by correlation coefficient of the environmental variable (Table S3).

FIG 3

Taxonomic affiliation of bacterial (phylum level) (A) and fungal sequences at the phylum level (B) and family level (C and D) in high-Se (>30 mg/kg) and low-Se (<30 mg/kg) soils. A comparison of the bacterial and fungal taxonomic affiliations with respect to mined and reference soils and samples collected in 2015 and 2016 is presented in Fig. S4.

FIG 4

Bacterial (A) and fungal (B) operational taxonomic units (OTUs) present in significantly greater relative abundances (adjusted P < 0.05) in high-Se soils than in low-Se soils.