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

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 (∼1.24 Mb), short average gene length (822 bp), 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.

Integrative modeling of gene and genome evolution roots the archaeal tree of life

“…The first DPANN to be characterized, Nanoarchaeum equitans, is obligately dependent on the crenarchaeote Ignicoccus hospitalis for growth (33), and other members of the group also have been observed in direct contact with larger archaeal cells (34), suggesting that symbiotic or parasitic lifestyles may be a common feature of the DPANN lineage. Nevertheless, genome analyses suggest that at least some members of the group might be capable of a free-living lifestyle (35).…”

Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics

“…Although candidate phyla are typically of low abundance, that is, part of the 'rare biosphere' (Sogin et al, 2006;Elshahed et al, 2008), they are prominent members of microbial communities in several different environments (Harris et al, 2004;Chouari et al, 2005;Vick et al, 2010;Peura et al, 2012;Cole et al, 2013;Farag et al, 2014;Gies et al, 2014;Parkes et al, 2014) and may have important ecological roles (Sekiguchi, 2006;Yamada et al, 2011). SAG sequencing and metagenomics have yielded partial, nearly-complete or complete genomes for close to 20 candidate bacterial phyla (Glöckner et al, 2010;Siegl et al, 2011;Youssef et al, 2011;Takami et al, 2012;Wrighton et al, 2012;Dodsworth et al, 2013;Kantor et al, 2013;McLean et al, 2013;Rinke et al, 2013;Kamke et al, 2014;Wrighton et al, 2014), as well as several major uncultivated lineages of Archaea (Elkins et al, 2008;Baker et al, 2010;Ghai et al, 2011;Nunoura et al, 2011;Narasingarao et al, 2012;Kozubal et al, 2013;Rinke et al, 2013;Youssef et al, 2015), opening a genomic window to a much better understanding of this so-called 'microbial dark matter' (Marcy et al, 2007;Rinke et al, 2013). In addition to individual organismal analyses, comparison of genomes from different habitats and from different lineages within a given candidate phylum can yield insight into the phylogeny, conserved features and metabolic diversity within these widespread but poorly understood branches on the tree of life <...>…”

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

“…Great attention has thus been paid to gene and/or genome duplication, which represent dominant forces for functional innovation, including neofunctionalization and subfunctionalization (6,7). Furthermore, the HGT process is considered a prevalent evolutionary mechanism that contributes to genomic diversification, species-level identification, and a trophic lifestyle (8,9). Recently, large-scale studies based on increasing genomic data have significantly expanded the spectrum of genome reduction into a pervasive source of genetic modifications that potentially cause adaptive phenotypic diversity (10).…”