Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity

Abstract

BackgroundThe current view suggests that in low-temperature acidic environments, archaea are significantly less abundant than bacteria. Thus, this study of the microbiome of Parys Mountain (Anglesey, UK) sheds light on the generality of this current assumption. Parys Mountain is a historically important copper mine and its acid mine drainage (AMD) water streams are characterised by constant moderate temperatures (8–18 °C), extremely low pH (1.7) and high concentrations of soluble iron and other metal cations.ResultsMetagenomic and SSU rRNA amplicon sequencing of DNA from Parys Mountain revealed a significant proportion of archaea affiliated with Euryarchaeota, which accounted for ca. 67% of the community. Within this phylum, potentially new clades of Thermoplasmata were overrepresented (58%), with the most predominant group being “E-plasma”, alongside low-abundant Cuniculiplasmataceae, ‘Ca. Micrarchaeota’ and ‘Terrestrial Miscellaneous Euryarchaeal Group’ (TMEG) archaea, which were phylogenetically close to Methanomassilicoccales and clustered with counterparts from acidic/moderately acidic settings. In the sediment, archaea and Thermoplasmata contributed the highest numbers in V3-V4 amplicon reads, in contrast with the water body community, where Proteobacteria, Nitrospirae, Acidobacteria and Actinobacteria outnumbered archaea. Cultivation efforts revealed the abundance of archaeal sequences closely related to Cuniculiplasma divulgatum in an enrichment culture established from the filterable fraction of the water sample. Enrichment cultures with unfiltered samples showed the presence of Ferrimicrobium acidiphilum, C. divulgatum, ‘Ca. Mancarchaeum acidiphilum Mia14’, ‘Ca. Micrarchaeota’-related and diverse minor (< 2%) bacterial metagenomic reads.ConclusionContrary to expectation, our study showed a high abundance of archaea in this extremely acidic mine-impacted environment. Further, archaeal populations were dominated by one particular group, suggesting that they are functionally important. The prevalence of archaea over bacteria in these microbiomes and their spatial distribution patterns represents a novel and important advance in our understanding of acidophile ecology. We also demonstrated a procedure for the specific enrichment of cell wall-deficient members of the archaeal component of this community, although the large fraction of archaeal taxa remained unculturable. Lastly, we identified a separate clustering of globally occurring acidophilic members of TMEG that collectively belong to a distinct order within Thermoplasmata with yet unclear functional roles in the ecosystem.Electronic supplementary materialThe online version of this article (10.1186/s40168-019-0623-8) contains supplementary material, which is available to authorized users.

A Deeper Look into the Biodiversity of the Extremely Acidic Copahue volcano-Río Agrio System in Neuquén, Argentina

“…For instance, the OTUs associated with Acidithiobacillus, Leptospirillum, Clostridiales, the Deltaproteobacteria genus Sva0485_ge, and the archaeal OTUs associated with Ferroplasma, E-plasma, and Thermoplasmataceae were 100-99% similar to sequences retrieved from an acid mine drainage from metal-rich abandoned tailing ponds in Tongling, China [39]. Similarly, sequences related to the OTUs affiliated with Acidithiobacillus, Leptospirillum, Acidibacillus, Metallibacterium, Deltaproteobacteria genus Sva0485_ge, Acidiphilium, Thermoplasmataceae, and E-plasma were obtained from the naturally acidic river Rio Tinto in Spain [3,4], while other sequences associated with Leptospirillum, Acidiphilium, Metallibacterium, Thermoplasmataceae, and E-plasma were retrieved from the extremely acidic environment of the Parys Mountain copper mine in United Kingdom [45]. To locate the sites where the microorganisms associated to the Copahue volcano-Rio Agrio OTUs have been isolated, we constructed a map ( Figure 4) and classified those environments in eight categories: Acid mine drainage (AMD), mine, wastewater, riverine, volcanic, hydrothermal, bioprocess, and other natural environment.…”

Explorative meta-analysis of 417 extant archaeal genomes to predict their contribution to the total microbiome functionality

“…Increases in archaeal abundance were found in extreme niches such as acidity and low temperature (Korzhenkov et al, 2019). Functionally, archaea play key roles in global carbon (e.g., methanogenesis or CO2 fixation) and nitrogen (e.g., N2 fixation or oxidation of ammonia) cycles (Leininger et al, 2006) but they also have complex relationships with both bacteria and fungi (Bengtson et al, 2012).…”

Quantifying the efficiency and biases of forest Saccharomyces sampling strategies

“…Enrichment culturing is a reliable and frequently used method for isolating difficult-to-culture bacteria, archaea, and eukaryotic microbes, including Saccharomyces, from natural environments (Korzhenkov et al, 2019;Li, Podar, & Morgan-Kiss, 2016;Schlegel & Jannasch, 1967;Sniegowski, Dombrowski, & Fingerman, 2002;Figure 1a). Microbiologists have been relying on enrichment cultures for over a century (Beijernick, 1961) and have used them to isolate many of the model Saccharomyces strains commonly used in laboratory studies (Johnson et al, 2004;Liti et al, 2009;Sniegowski et al, 2002).…”