\u2018ARMAN\u2019 archaea depend on association with euryarchaeal host in culture and in situ

Olga V Golyshina,Ilya V Kublanov,Stepan V Toshchakov,Michail M Yakimov,Violetta La Cono,Sergey N Gavrilov,Erika Arcadi,Peter N Golyshin,Manuel Ferrer,Kira S Makarova,Taras Y Nechitaylo,Aleksei A Korzhenkov,Yuri I Wolf

doi:10.1038/s41467-017-00104-7

Abstract

Intriguing, yet uncultured ‘ARMAN’-like archaea are metabolically dependent on other members of the microbial community. It remains uncertain though which hosts they rely upon, and, because of the lack of complete genomes, to what extent. Here, we report the co-culturing of ARMAN-2-related organism, Mia14, with Cuniculiplasma divulgatum PM4 during the isolation of this strain from acidic streamer in Parys Mountain (Isle of Anglesey, UK). Mia14 is highly enriched in the binary culture (ca. 10% genomic reads) and its ungapped 0.95 Mbp genome points at severe voids in central metabolic pathways, indicating dependence on the host, C. divulgatum PM4. Analysis of C. divulgatum isolates from different sites and shotgun sequence data of Parys Mountain samples suggests an extensive genetic exchange between Mia14 and hosts in situ. Within the subset of organisms with high-quality genomic assemblies representing the ‘DPANN’ superphylum, the Mia14 lineage has had the largest gene flux, with dozens of genes gained that are implicated in the host interaction.

Highlights

Intriguing, yet uncultured ‘ARMAN’-like archaea are metabolically dependent on other members of the microbial community
Emerging findings from metagenomic data sets of ARMAN-like archaea and especially their ubiquity suggest that this group plays important roles in the environment, the exact roles have yet to be established[2].The phylogenomic placement of archaea from this group still represents a matter for discussion[5,6,7]
Using data on archaeal Clusters of Orthologous Groups (arCOGs) gains and losses, we reconstructed its evolutionary trajectory starting from the last archaeal common ancestor (LACA), which pointed at Mia[14] having the greatest known extent of gene fluxes within the ‘DPANN’ superphylum

Summary

Introduction

Intriguing, yet uncultured ‘ARMAN’-like archaea are metabolically dependent on other members of the microbial community It remains uncertain though which hosts they rely upon, and, because of the lack of complete genomes, to what extent. Detected at Iron Mountain (California, USA), these archaeal lineages were subsequently confirmed to occur in various acid mine drainage (AMD) systems[2] We report the co-cultivation and analysis of the ungapped genome of an ARMAN-like organism, the ‘Candidatus Mancarchaeum acidiphilum’ Mia[14], which was enriched in the laboratory binary culture with Cuniculiplasma divulgatum PM4, a recently described representative of the family Cuniculiplasmataceae within Thermoplasmata[15]. Using data on arCOGs gains and losses, we reconstructed its evolutionary trajectory starting from the last archaeal common ancestor (LACA), which pointed at Mia[14] having the greatest known extent of gene fluxes within the ‘DPANN’ superphylum

Methods

Results

Conclusion