Unexpected predominance of Archaea in a cool hyperacidic environment.

When we came for first time to sample Parys Mountain old copper mine on the Isle of Anglesey, we did not expect that a tiny stream would become a real treasure chest.
Published in Microbiology
Unexpected predominance of Archaea in a cool hyperacidic environment.
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Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity - Microbiome

Background The 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. Results Metagenomic 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. Conclusion Contrary 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.

From this very acidic site (pH 1.3-1.6) we have isolated and characterised a new archaeal genus and species,  Cuniculiplasma divulgatum from a new family Cuniculiplasmataceae (order Thermoplasmatales). Comparative genomic analysis of Cuniculiplasma strains, which we isolated from Parys Mountain and Iberian pyritic belt site and a metagenomic assembly from a sibling organism from California pointed at a remarkable degree of conservation in their genomes (1,2).

Later, we described the association between C. divulgatum and its ectosymbiont (or ectoparasite) “Candidatus Mancarchaeum acidiphilum” (“Micrarchaeota”) and reported on the analysis and evolutionary patterns of this first ungapped genome in DPANN Superphylum (3). It was quite logical that our next step towards better understanding of microbial diversity of this hyperacidic ecosystem would be the assessment of the entire acidophilic microbiome and spatial distribution of microorganisms inhabiting water and sediment subsystems.

Shotgun metagenomics and SSU rRNA amplicon sequencing of DNA samples revealed that Euryarchaeota accounted for 67 % from the whole community, with the prevalence of Thermoplasmata (58%). Within Thermoplasmata, one particular group, “E-plasma”, without isolated representatives was in a majority (up to 43.5 % of total metagenomic reads) (Fig).

Among archaeal taxa, Cuniculiplasmataceae, “Candidatus Micrarchaeota” and “Terrestrial Miscellaneous Euryarchaeal Group” (TMEG) archaea were present in low numbers. TMEG archaea were earlier considered an “environmental clade” linked to Methanomassilicoccales-related archaea (4). Our global phylogenetic analysis of TMEG archaea showed strong clustering of Parys Mountain clonal variants with sequences detected in other acidic and moderately acidic places, pointing at the affiliation of this group with a new order within Thermoplasmata.

We also observed that this group of acidophilic organisms was often overlooked in acidic microbiomes. Highest numbers of archaea and in particular, Thermoplasmata were found in sediment samples, in contrast to the aqueous subsystem, where bacteria were in the majority. Furthermore, our analysis of microbial diversity in enrichment cultures pointed at the significance of sample pre-treatment, which could be used for isolation of cell wall-deficient archaea.

Overall, our results were counterintuitive: it is commonly accepted that acidophilic bacteria dominate low- and moderate-temperature environments, exemplified by Parys Mountain, which is exposed to the cool maritime climate. Many questions related to acidophilic Thermoplasmata still need to be addressed, e.g. the functions of predominant and “rare” community members and the reason of a very limited fraction of Thermoplasmata being cultured. Therefore, we are looking forward to sampling Parys Mountain in the near future. 

1.Golyshina, O.V. et al. The novel extremely acidophilic, cell-wall-deficient archaeon Cuniculiplasma divulgatum gen. nov., sp. nov. represents a new family, Cuniculiplasmataceae fam. nov., of the order Thermoplasmatales. Int J Syst Evol Microbiol. 66(1), 332-40 (2016a).

2. Golyshina, O.V. et al. Biology of archaea from a novel family Cuniculiplasmataceae (Thermoplasmata) ubiquitous in hyperacidic environments. Sci Rep. 6, 39034 (2016b).

3. Golyshina, O.V. et al. “ARMAN” archaea depend on association with euryarchaeal host in culture and in situ. Nat Commun. 8, 60 (2017).

4. Söllinger, A. et al. Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiol Ecol. 92(1), fiv149 (2016).

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