Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park

Abstract

Geothermal systems in Yellowstone National Park (YNP) provide an outstanding opportunity to understand the origin and evolution of metabolic processes necessary for life in extreme environments including low pH, high temperature, low oxygen and elevated concentrations of reduced iron. Previous phylogenetic studies of acidic ferric iron mats from YNP have revealed considerable diversity of uncultivated and undescribed archaea. The goal of this study was to obtain replicate de novo genome assemblies for a dominant archaeal population inhabiting acidic ironoxide mats in YNP. Detailed analysis of conserved ribosomal and informational processing genes indicates that the replicate assemblies represent a new candidate phylum within the domain Archaea referred to here as 'Geoarchaeota' or 'novel archaeal group 1 (NAG1)'. The NAG1 organisms contain pathways necessary for the catabolism of peptides and complex carbohydrates as well as a bacterial-like Form I carbon monoxide dehydrogenase complex likely used for energy conservation. Moreover, this novel population contains genes involved in the metabolism of oxygen including a Type A heme copper oxidase, a bd-type terminal oxidase and a putative oxygen-sensing protoglobin. NAG1 has a variety of unique bacterial-like cofactor biosynthesis and transport genes and a Type3-like CRISPR system. Discovery of NAG1 is critical to our understanding of microbial community structure and function in extant thermophilic iron-oxide mats of YNP, and will provide insight regarding the evolution of Archaea in early Earth environments that may have important analogs active in YNP today.

Carbon Dioxide Fixation by Metallosphaera yellowstonensis and Acidothermophilic Iron-Oxidizing Microbial Communities from Yellowstone National Park

“…Other archaea present in these communities include members of two novel archaeal groups, the Thaumarchaeota and the Euryarchaeota (Thermoplasmatales-like), as well as other crenarchaea within the orders Thermoproteales and Desulfurococcales (19,24,25). However, sequence assemblies corresponding to these populations do not contain evidence of marker genes for known CO 2 fixation pathways and appear to be primarily heterotrophic (18,19,24,25,37,41). Despite the diversity of archaea in these Fe(II)-oxidizing communities, the only known CO 2 fixation pathways found in metagenome sequence analyses included the 3-HP/4-HB pathway (contributed by M. yellowstonensis-like and other Sulfolobales populations) and the r-TCA cycle (contributed by Hydrogenobaculum-like populations).…”

“…These microbial communities represent a consortium of numerous archaea, including several crenarchaeal populations (orders Sulfolobales, Desulfurococcales, and Thermoproteales) and representatives of the candidate phylum Geoarchaeota (18)(19)(20), as well as acidophilic bacteria from the order Aquificales. Hydrogenobaculum spp.…”

Physiology, Biochemistry, and Applications of F420- and Fo-Dependent Redox Reactions

“…The cofactor is also proposed to be central to the metabolism of the various lineages of the anaerobic methanotrophic archaea (ANME) (21,137). Comparative genomics indicate that the genes required for F 420 biosynthesis are also distributed in the Thaumarchaeota, Aigarchaeota, Geoarchaeota, Bathyarchaeota, and Lokiarchaeota (138)(139)(140)(141)(142). The absorbance spectra of single cells of the ammonia-and cyanate-oxidizing thaumarchaeon Nitrososphaera gargensis are also consistent with the presence of F 420 (143,144).…”

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 <...>…”