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Open AccessArticle

Metagenomic and Metatranscriptomic Study of Microbial Metal Resistance in an Acidic Pit Lake

1
Department of Civil and Environmental Engineering, The Pennsylvania State University, 212 Sackett Building, University Park, PA 16802, USA
2
Geochemistry and Sustainable Mining Unit, Instituto Geológico y Minero de España (IGME), Calera 1, Tres Cantos, 28760 Madrid, Spain
3
Department of Ecosystem Science and Management, The Pennsylvania State University, 450 ASI, University Park, PA 16802, USA
4
Environment & Sustainability Institute and Camborne School of Mines, University of Exeter, Penryn Campus, Penryn TR10 9FE, UK
5
Department of Geosciences, The Pennsylvania State University, 211 Deike Building, University Park, PA 16802, USA
*
Author to whom correspondence should be addressed.
Microorganisms 2020, 8(9), 1350; https://doi.org/10.3390/microorganisms8091350
Received: 1 August 2020 / Revised: 18 August 2020 / Accepted: 2 September 2020 / Published: 4 September 2020
(This article belongs to the Special Issue Extremophiles 2.0)
Cueva de la Mora (CM) is an acidic, meromictic pit lake in the Iberian Pyrite Belt characterized by extremely high metal(loid) concentrations and strong gradients in oxygen, metal, and nutrient concentrations. We hypothesized that geochemical variations with depth would result in differences in community composition and in metal resistance strategies among active microbial populations. We also hypothesized that metal resistance gene (MRG) expression would correlate with toxicity levels for dissolved metal species in the lake. Water samples were collected in the upper oxic layer, chemocline, and deep anoxic layer of the lake for shotgun metagenomic and metatranscriptomic sequencing. Metagenomic analyses revealed dramatic differences in the composition of the microbial communities with depth, consistent with changing geochemistry. Based on relative abundance of taxa identified in each metagenome, Eukaryotes (predominantly Coccomyxa) dominated the upper layer, while Archaea (predominantly Thermoplasmatales) dominated the deep layer, and a combination of Bacteria and Eukaryotes were abundant at the chemocline. We compared metal resistance across communities using a curated list of protein-coding MRGs with KEGG Orthology identifiers (KOs) and found that there were broad differences in the metal resistance strategies (e.g., intracellular metal accumulation) expressed by Eukaryotes, Bacteria, and Archaea. Although normalized abundances of MRG and MRG expression were generally higher in the deep layer, expression of metal-specific genes was not strongly related to variations in specific metal concentrations, especially for Cu and As. We also compared MRG potential and expression in metagenome assembled genomes (MAGs) from the deep layer, where metal concentrations are highest. Consistent with previous work showing differences in metal resistance mechanisms even at the strain level, MRG expression patterns varied strongly among MAG populations from the same depth. Some MAG populations expressed very few MRG known to date, suggesting that novel metal resistance strategies remain to be discovered in uncultivated acidophiles. View Full-Text
Keywords: metal toxicity; metal resistance; acidophiles; metagenomics; metatranscriptomics; acidic systems; Cueva de la Mora; Iberian Pyrite Belt metal toxicity; metal resistance; acidophiles; metagenomics; metatranscriptomics; acidic systems; Cueva de la Mora; Iberian Pyrite Belt
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MDPI and ACS Style

Ayala-Muñoz, D.; Burgos, W.D.; Sánchez-España, J.; Couradeau, E.; Falagán, C.; Macalady, J.L. Metagenomic and Metatranscriptomic Study of Microbial Metal Resistance in an Acidic Pit Lake. Microorganisms 2020, 8, 1350.

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