A stratified microbial community from abandoned polymetallic mine tailings in Western Australia, characterized by vertical zonation of acidophilic and anaerobic organisms across steep pH and redox gradients. This system represents a naturally acidifying sulfidic tailings dump where oxidative weathering of Pb-Zn sulfide minerals drives extreme environmental heterogeneity and microhabitat specialization. The upper oxidized layer (pH 1.5-3.0) is dominated by iron- and sulfur-oxidizing acidophiles including Acidithiobacillus ferrooxidans (dual Fe/S oxidation) and Leptospirillum ferriphilum (specialized Fe oxidation), which generate ferric iron and sulfuric acid that mobilize lead, zinc, copper, and iron from sulfide minerals including galena (PbS), sphalerite (ZnS), and chalcopyrite (CuFeS₂). The intermediate chemocline exhibits dramatic pH transitions (pH 3-5) where Ferroplasma acidarmanus thrives in highly acidic microniches while facultative acidophiles transition to neutral conditions. The deeper sediment layer (pH 5-7) harbors anaerobic metal-reducing bacteria including Geobacter metallireducens that reduce ferric iron to ferrous iron using organic carbon, creating redox cycling between oxic and anoxic zones. Metagenome-assembled genomes (MAGs) reveal extensive microhabitat partitioning, with distinct populations specializing in surface oxidation, chemocline transitions, or deep anaerobic processes. Metal concentrations reach toxic levels (Pb: hundreds mg/kg, Zn: thousands mg/kg, Cu: hundreds mg/kg, Fe: up to 30% w/w), selecting for metal-resistant populations. This abandoned tailings system demonstrates natural biogeochemical cycling without active mining, with microbial communities driving ongoing metal mobilization (upper layers) and potential natural attenuation (deeper layers). The MAG-resolved metagenomics approach reveals cryptic microbial diversity including novel acidophilic lineages adapted to polymetallic stress, providing insights into bioremediation strategies and microbial evolution in extreme anthropogenic environments.
Taxonomy
| Taxon | Ontology ID | Functional Roles | Abundance |
|---|---|---|---|
| Acidithiobacillus ferrooxidans | NCBITaxon:920 |
PRIMARY_DEGRADER
|
DOMINANT |
| Leptospirillum ferriphilum | NCBITaxon:178606 |
PRIMARY_DEGRADER
|
DOMINANT |
| Ferroplasma acidarmanus | NCBITaxon:97393 |
PRIMARY_DEGRADER
CROSS_FEEDER
|
ABUNDANT |
| Geobacter metallireducens | NCBITaxon:28232 |
SECONDARY_FERMENTER
|
COMMON |
| Sulfobacillus thermosulfidooxidans | NCBITaxon:28034 |
PRIMARY_DEGRADER
|
RARE |
| Acidiphilium cryptum | NCBITaxon:524 |
CROSS_FEEDER
|
COMMON |
Ecological Interactions
Lead and Zinc Mobilization from Sulfide Minerals
MUTUALISMSource Taxon: Acidithiobacillus ferrooxidans
Metabolites: galena (CHEBI:82328), sphalerite (CHEBI:82332), Fe(III) (CHEBI:29034), lead(2+) (CHEBI:49807), zinc(2+) (CHEBI:29105), sulfuric acid (CHEBI:26836)
Biological Processes:
- oxidation-reduction process (GO:0055114)
- iron ion transport (GO:0006826)
- response to metal ion (GO:0010038)
Evidence
-
doi:10.1128/aem.02458-10 - SUPPORT (IN_VIVO)"Analysis of spatial and temporal variations in the microbial community in the abandoned tailings impoundment of a Pb-Zn mine revealed distinct microbial populations associated with the different oxidation stages of the tailings"
-
PMID:22092956 - SUPPORT (IN_VIVO)"Weathering of waste rock, high in S and Fe, had resulted in a varying elemental dispersal down a face of the tailings hill"
Stratified Iron Redox Cycling
COMMENSALISMSource Taxon: Leptospirillum ferriphilum
Metabolites: Fe(II) (CHEBI:29033), Fe(III) (CHEBI:29034), ferrihydrite (CHEBI:82823)
Biological Processes:
- oxidation-reduction process (GO:0055114)
- iron ion transport (GO:0006826)
- dissimilatory iron reduction (GO:0019568)
Evidence
-
doi:10.1016/j.jhazmat.2023.130774 - SUPPORT (IN_VIVO)"Specifically, key genes involved in sulfur and iron oxidation were significantly enriched in the surface tailings, whereas those associated with reductive nitrogen, sulfur, and iron processes were enriched in the deeper layers"
-
doi:10.1016/j.scitotenv.2021.151468 - SUPPORT (IN_VIVO)"DNA hypermethylation caused by environmental pollutants like cadmium (Cd) has already been demonstrated in many invertebrates, including earthworms"
Microhabitat Specialization Along pH Gradient
COMMENSALISMSource Taxon: Ferroplasma acidarmanus
Metabolites: hydron (CHEBI:15378)
Biological Processes:
- response to pH (GO:0009268)
- cellular pH homeostasis (GO:0030641)
- response to metal ion (GO:0010038)
Evidence
-
doi:10.1128/aem.02883-07 - SUPPORT (IN_VIVO)"Phylotype richness in these communities decreased from 42 in the OS control to 24 in the moderately acidic samples and 8 in the extremely acidic tailing samples"
-
doi:10.1128/aem.00294-14 - SUPPORT (IN_VIVO)"Together, these results suggest that pH is primarily responsible for structuring whole communities in the extreme and heterogeneous mine tailings, although the diverse microbial taxa may respond differently to various environmental conditions."
Copper Mobilization and Toxicity Interactions
COMPETITIONSource Taxon: Acidithiobacillus ferrooxidans
Metabolites: chalcopyrite (CHEBI:50831), copper(2+) (CHEBI:29036)
Biological Processes:
- copper ion transport (GO:0006825)
- response to copper ion (GO:0046688)
- oxidation-reduction process (GO:0055114)
Evidence
-
doi:10.3390/min14030255 - SUPPORT (IN_VITRO)"The study examined the solubilisation process using a mesophilic mixed bacterial culture, including Acidithiobacillus ferrooxidans (AF), Acidithiobacillus thiooxidans (AT), Leptospirillum ferrooxidans (LF), and the thermophilic species Sulfobacillus thermosulfidooxidans (ST)"
-
PMID:22092956 - SUPPORT (IN_VIVO)"Weathering of waste rock, high in S and Fe, had resulted in a varying elemental dispersal down a face of the tailings hill"
Environmental Factors
| Factor | Value | Unit |
|---|---|---|
| pH Stratification | 1.5-7.0 | pH units (depth-dependent) |
| Lead Concentration | 200-800 | mg/kg solid phase; 5-50 mg/L dissolved |
| Zinc Concentration | 2000-8000 | mg/kg solid phase; 50-500 mg/L dissolved |
| Copper Concentration | 300-1200 | mg/kg solid phase; 20-150 mg/L dissolved |
| Iron Concentration | Up to 30% | % w/w solid phase; 1000-10000 mg/L dissolved |
| Oxygen Stratification | Oxic to anoxic | depth-dependent gradient |
| Arid Climate with Wetting-Drying Cycles | Semi-arid | climate classification |
| MAG Diversity and Specialization | 100-200 | estimated distinct MAG populations |
| Time Since Abandonment | Decades | years since mining cessation |