Unexpected Dominance of Elusive Acidobacteria in Early Industrial Soft Coal Slags

Abstract

Acid mine drainage (AMD) and mine tailing environments are well-characterized ecosystems known to be dominated by organisms involved in iron- and sulfur-cycling. Here we examined the microbiology of industrial soft coal slags that originate from alum leaching, an ecosystem distantly related to AMD environments. Our study involved geochemical analyses, bacterial community profiling, and shotgun metagenomics. The slags still contained high amounts of alum constituents (aluminum, sulfur), which mediated direct and indirect effects on bacterial community structure. Bacterial groups typically found in AMD systems and mine tailings were not present. Instead, the soft coal slags were dominated by uncharacterized groups of Acidobacteria (DA052 [subdivision 2], KF-JG30-18 [subdivision 13]), Actinobacteria (TM214), Alphaproteobacteria (DA111), and Chloroflexi (JG37-AG-4), which have previously been detected primarily in peatlands and uranium waste piles. Shotgun metagenomics allowed us to reconstruct 13 high-quality Acidobacteria draft genomes, of which two genomes could be directly linked to dominating groups (DA052, KF-JG30-18) by recovered 16S rRNA gene sequences. Comparative genomics revealed broad carbon utilization capabilities for these two groups of elusive Acidobacteria, including polysaccharide breakdown (cellulose, xylan) and the competence to metabolize C1 compounds (ribulose monophosphate pathway) and lignin derivatives (dye-decolorizing peroxidases). Equipped with a broad range of efflux systems for metal cations and xenobiotics, DA052 and KF-JG30-18 may have a competitive advantage over other bacterial groups in this unique habitat.

Lanthanide-Dependent Methylotrophs of the Family Beijerinckiaceae : Physiological and Genomic Insights

“…Phylogenetic and phylogenomic analysis. Early-industrial soft coal slags, resulting from the extraction of aluminum sulfur minerals, were recently described as an unusual habitat for microbial life (42). We isolated three pure cultures of methylotrophic bacteria using these aluminum-rich soft coal slags as an inoculum.…”

“…(C) The bioavailable fraction of lanthanides present in the sampled slag material was assessed by total digestion plus ICP-MS to determine the absolute quantities of lanthanides present (see Table S4 in the supplemental material) and by sequential digestion plus ICP-MS. We define bioavailable here as fractions I (mobile) and II (exchangeable) according to the sequential digestion method of Zeien and Brümmer (53,89). The nomenclature for the sampling sites is according to Wegner and Liesack (42). RH1 and RH2 refer to slag deposition sites from which the slag material that was used for isolation was collected.…”

“…The pH of the reference forest soil is near neutral (pH 6.8). The slag material featured elevated levels of aluminum, iron, and sulfur (42).…”

“…In the present work, we used soft coal slags, which are residuals of early-industrial mineral leaching (42) and feature an increased load of mobilizable lanthanides, as starting material for the isolation of microorganisms. We assumed that the increased availability of lanthanides might favor microbes that are able to utilize them.…”

Recent Understanding of Soil Acidobacteria and Their Ecological Significance: A Critical Review

“…Genomic studies highlight the carbohydrate utilization potential exhibited by Acidobacteria members (Ward et al, 2009;Kielak et al, 2016a). The presence of genes encoding enzymes for the degradation of complex carbohydrate polymers like cellulose, hemicellulose, chitin, xylan, and lignin derivatives signifies their active participation in the carbon circuit as decomposers in soil (Ward et al, 2009;Wegner and Liesack, 2017;Banerjee et al, 2018;Belova et al, 2018) and cycling of organic matter derived from plants, fungi, and insects (King and Weber, 2007;García-Fraile et al, 2016;Dedysh and Damsté, 2018).…”