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El Chichón volcano is one of the most active volcanoes in Mexico. Previous studies have described its poly-extreme conditions and its bacterial composition, although the functional features of the complete microbiome have not been characterized yet. By using metabarcoding analysis, metagenomics, metabolomics and enzymology techniques, the microbiome of the crater lake was characterized in this study. New information is provided on the taxonomic and functional diversity of the representative Archaea phyla, Crenarchaeota and Euryarchaeota, as well as those that are representative of Bacteria, Thermotogales and Aquificae. With culture of microbial consortia and with the genetic information collected from the natural environment sampling, metabolic interactions were identified between prokaryotes, which can withstand multiple extreme conditions. The existence of a close relationship between the biogeochemical cycles of carbon and sulfur in an active volcano has been proposed, while the relationship in the energy metabolism of thermoacidophilic bacteria and archaea in this multi-extreme environment was biochemically revealed for the first time. These findings contribute towards understanding microbial metabolism under extreme conditions, and provide potential knowledge pertaining to "microbial dark matter", which can be applied to biotechnological processes and evolutionary studies.

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The ability to establish biofilms is a key trait for microorganisms growing in extreme environments. The extracellular polymeric substances (EPS) present in biofilms provide not only surface attachment, but also protection against all kinds of environmental stressors, including desiccation, salinity, temperature or heavy metal pollution. The acquisition of suitable biofilm characteristics might thus be an important process mediating the adaptation of microorganisms to novel environmental conditions. In this work we have characterized the EPS of 20 phylogenetically diverse biofilms collected in situ from five contrasting extreme environments, including two geothermal areas (Copahue, Argentina; Seltun, Iceland), two cold areas (Pastoruri glacier, Peru; Byers Peninsula, Antarctica) and one extremely acidic river (Río Tinto, Spain). Biofilms were subjected to biochemical characterization, glycan profiling and immunoprofiling with an antibody microarray. Our results showed that environmental conditions strongly influence biofilm characteristics, with microorganisms from the same environment achieving similar EPS compositions regardless of the phylogeny of their main species. The concentration of some monosaccharides in the EPS could be related to environmental conditions such as temperature or heavy metal toxicity, suggesting that in some cases stress resistance can be mediated by specific sugars. Overall, our results highlight the existence of conserved EPS compositional patterns for each extreme environment, which could in turn be exploited to engineer ecological adaptations in genetically modified microorganisms.

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The generation of acid rock drainage (ARD) was observed in an area of Nevado Pastoruri as a result of the oxidative dissolution of pyrite-rich lutites and sandstones. These ARDs are generated as abundant pyrite becomes exposed to atmospheric conditions as a result of glacier retreat. The proglacial zone contains lagoons, springs, streams and wetlands, scant vegetation, and intense fluvioglacial erosion. This work reports a comprehensive identification and the results of sampling of the lagoons and springs belonging to the microbasin, which is the headwaters of the Pachacoto River, as well as mapping results based on the hydrochemical data obtained in our study. The physical properties and water chemistry of 12 springs and 22 lagoons from the proglacial zone are also presented. Water springs are far from being chemically uniform, with pH and EC values ranging between 2.55-6.42 and 23-1110 µS/cm respectively, which suggests a strong geologic control on water chemistry. Fe-SO4-2 concentrations confirm the intense process of pyrite oxidative dissolution. Many of the lagoons are affected by ARD, with low pH (~ 3), and high EC (256-1092 µS/cm) values when compared with unaffected lagoons (EC between 7 and 59 µS/cm), indicating a high degree of mineralization. The affected lagoons show higher concentrations of SO42- and SiO2, and elements as Fe, Al, Mg, Mn, Zn, Co, and Ni, which are related to the alteration of pyrite and the dissolution of aluminosilicate minerals. Schwertmannite-goethite appears to be the most important mineral phases controlling the Fe solubility at a pH of 2-3.5. Moreover, they act as a sorbent of trace elements (As, Sb, V, Pb, Zn, Cr), which is an efficient mechanism of natural attenuation. Despite of this, the water flowing out from the basin is acid (pH 3.1) and contains significant concentrations of Fe (0.98 mg/L) and Al (3.76 mg/L) that confer mineral acidity to water. The Pachacoto River located 5.5 km downstream from this point showed a strong natural attenuation, with a pH of 6.9 and low concentration of metals. This mitigating process is possible due to (i) the formation of precipitates that retain toxic elements and (ii) the mixing with natural waters that promote dilution, which favor the increase of pH until circumneutral conditions.

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The exposure of fresh sulfide-rich lithologies by the retracement of the Nevado Pastoruri glacier (Central Andes, Perú) is increasing the presence of heavy metals in the water as well as decreasing the pH, producing an acid rock drainage (ARD) process in the area. We describe the microbial communities of an extreme ARD site in Huascarán National Park as well as their correlation with the water physicochemistry. Microbial biodiversity was analyzed by FLX 454 sequencing of the 16S rRNA gene. The suggested geomicrobiological model of the area distinguishes three different zones. The proglacial zone is located in the upper part of the valley, where the ARD process is not evident yet. Most of the OTUs detected in this area were related to sequences associated with cold environments (i.e., psychrotolerant species of Cyanobacteria or Bacteroidetes). After the proglacial area, an ARD-influenced zone appeared, characterized by the presence of phylotypes related to acidophiles (Acidiphilium) as well as other species related to acidic and cold environments (i.e., acidophilic species of Chloroflexi, Clostridium and Verrumicrobia). Sulfur- and iron-oxidizing acidophilic bacteria (Acidithiobacillus) were also identified. The post-ARD area was characterized by the presence of OTUs related to microorganisms detected in soils, permafrost, high mountain environments, and deglaciation areas (Sphingomonadales, Caulobacter or Comamonadaceae).

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Copahue is a natural geothermal field (Neuquén province, Argentina) dominated by the Copahue volcano. As a consequence of the sustained volcanic activity, Copahue presents many acidic pools, hot springs and solfataras with different temperature and pH conditions that influence their microbial diversity. The occurrence of microbial biofilms was observed on the surrounding rocks and the borders of the ponds, where water movements and thermal activity are less intense. Microbial biofilms are particular ecological niches within geothermal environments; they present different geochemical conditions from that found in the water of the ponds and hot springs which is reflected in different microbial community structure. The aim of this study is to compare microbial community diversity in the water of ponds and hot springs and in microbial biofilms in the Copahue geothermal field, with particular emphasis on Cyanobacteria and other photosynthetic species that have not been detected before in Copahue. In this study, we report the presence of Cyanobacteria, Chloroflexi and chloroplasts of eukaryotes in the microbial biofilms not detected in the water of the ponds. On the other hand, acidophilic bacteria, the predominant species in the water of moderate temperature ponds, are almost absent in the microbial biofilms in spite of having in some cases similar temperature conditions. Species affiliated with Sulfolobales in the Archaea domain are the predominant microorganism in high temperature ponds and were also detected in the microbial biofilms.

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The Copahue geothermal system is a natural extreme environment located at the northern end of the Cordillera de los Andes in Neuquén province in Argentina. The geochemistry and consequently the biodiversity of the area are dominated by the activity of the Copahue volcano. The main characteristic of Copahue is the extreme acidity of its aquatic environments; ponds and hot springs of moderate and high temperature as well as Río Agrio. In spite of being an apparently hostile location, the prokaryotic biodiversity detected by molecular ecology techniques as well as cultivation shows a rich and diverse environment dominated by acidophilic, sulphur oxidising bacteria or archaea, depending on the conditions of the particular niche studied. In microbial biofilms, found in the borders of the ponds where thermal activity is less intense, the species found are completely different, with a high presence of cyanobacteria and other photosynthetic species. Our results, collected during more than 10 years of work in Copahue, have enabled us to outline geomicrobiological models for the different environments found in the ponds and Río Agrio. Besides, Copahue seems to be the habitat of novel, not yet characterised autochthonous species, especially in the domain Archaea.