Original Article

The ISME Journal (2015) 9, 447–460; doi:10.1038/ismej.2014.141; published online 1 August 2014

Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’

Noha H Youssef1, Christian Rinke2, Ramunas Stepanauskas3, Ibrahim Farag1, Tanja Woyke2 and Mostafa S Elshahed1

  1. 1Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, OK, USA
  2. 2DOE Joint Genome Institute, Walnut Creek, CA, USA
  3. 3Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA

Correspondence: NH Youssef, Department of Microbiology and Molecular Genetics, Oklahoma State University, 1110S Innovation Way Drive, Stillwater, OK 74074, USA. E-mail: noha@okstate.edu

Received 1 May 2014; Revised 22 June 2014; Accepted 1 July 2014
Advance online publication 1 August 2014

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Abstract

The archaeal phylum ‘Diapherotrites’ was recently proposed based on phylogenomic analysis of genomes recovered from an underground water seep in an abandoned gold mine (Homestake mine in Lead, SD, USA). Here we present a detailed analysis of the metabolic capabilities and genomic features of three single amplified genomes (SAGs) belonging to the ‘Diapherotrites’. The most complete of the SAGs, Candidatus ‘Iainarchaeum andersonii’ (Cand. IA), had a small genome (~1.24Mb), short average gene length (822bp), one ribosomal RNA operon, high coding density (~90.4%), high percentage of overlapping genes (27.6%) and low incidence of gene duplication (2.16%). Cand. IA genome possesses limited catabolic capacities that, nevertheless, could theoretically support a free-living lifestyle by channeling a narrow range of substrates such as ribose, polyhydroxybutyrate and several amino acids to acetyl-coenzyme A. On the other hand, Cand. IA possesses relatively well-developed anabolic capabilities, although it remains auxotrophic for several amino acids and cofactors. Phylogenetic analysis suggests that the majority of Cand. IA anabolic genes were acquired from bacterial donors via horizontal gene transfer. We thus propose that members of the ‘Diapherotrites’ have evolved from an obligate symbiotic ancestor by acquiring anabolic genes from bacteria that enabled independent biosynthesis of biological molecules previously acquired from symbiotic hosts. ‘Diapherotrites’ 16S rRNA genes exhibit multiple mismatches with the majority of archaeal 16S rRNA primers, a fact that could be responsible for their observed rarity in amplicon-generated data sets. The limited substrate range, complex growth requirements and slow growth rate predicted could be responsible for its refraction to isolation.