The complete genome sequence and emendation of the hyperthermophilic, obligate iron-reducing archaeon “Geoglobus ahangari” strain 234T

Abstract

“Geoglobus ahangari” strain 234T is an obligate Fe(III)-reducing member of the Archaeoglobales, within the archaeal phylum Euryarchaeota, isolated from the Guaymas Basin hydrothermal system. It grows optimally at 88 °C by coupling the reduction of Fe(III) oxides to the oxidation of a wide range of compounds, including long-chain fatty acids, and also grows autotrophically with hydrogen and Fe(III). It is the first archaeon reported to use a direct contact mechanism for Fe(III) oxide reduction, relying on a single archaellum for locomotion, numerous curled extracellular appendages for attachment, and outer-surface heme-containing proteins for electron transfer to the insoluble Fe(III) oxides. Here we describe the annotation of the genome of “G. ahangari” strain 234T and identify components critical to its versatility in electron donor utilization and obligate Fe(III) respiratory metabolism at high temperatures. The genome comprises a single, circular chromosome of 1,770,093 base pairs containing 2034 protein-coding genes and 52 RNA genes. In addition, emended descriptions of the genus “Geoglobus” and species “G. ahangari” are described.Electronic supplementary materialThe online version of this article (doi:10.1186/s40793-015-0035-8) contains supplementary material, which is available to authorized users.

A Membrane-Bound Cytochrome EnablesMethanosarcina acetivoransto Conserve Energy to Support Growth from Extracellular Electron Transfer

“…The putative function of outer-surface cytochromes is terminal electron transfer to extracellular electron acceptors, similar to the role that outer surface c -type cytochromes play in extracellular electron transfer in Gram-negative bacteria such as Shewanella and Geobacter species (20–22). Similar c -type cytochrome electrical contacts have been proposed for Fe(III)-reducing Archaea such as Ferroglobus and Geoglobus species (23, 24). However, the study of the mechanisms for extracellular electron transfer in these archaea has been stymied by the lack of microorganisms available in pure culture that can grow via extracellular electron transfer and are genetically tractable.…”

“…A wide diversity of archaea are capable of extracellular electron transfer (72), but the mechanisms are poorly understood. For archaea such as Ferroglobus placidus (23), Geoglobus ahangari (24), and diverse ANME (13–19) it has been proposed that outer-membrane cytochromes are the terminal reductase. The rapid non-physiological reduction of extracellular electron acceptors by a range of redox-active proteins and co-factors in vitro necessitates genetically tractable model organisms for physiologically relevant functional studies.…”

MEBS, a software platform to evaluate large (meta)genomic collections according to their metabolic machinery: unraveling the sulfur cycle

“…Another 59 Sur organisms have been isolated from Sulfur-rich environments, such as hot springs or solfataric muds. Remarkably, some of this species include hard-to culture genomes reconstructed from metagenomic sequences such as Candidatus Desulforudis audaxviator MP104C isolated from basalt-hosted fluids of the deep subseafloor [6]; an unnamed endosymbiont of a scaly snail from a black smoker chimney [59] and archaeon Geoglobus ahangari, sampled from a 2,000m depth hydrothermal vent [60]. Furthermore, we also confirmed within Sur the implication of S-cycle of 20 species of the genus Campylobacter.…”

Divergent methyl-coenzyme M reductase genes in a deep-subseafloor Archaeoglobi

“…Alkane oxidation can be energetically favourable when coupled to an electron acceptor such as sulfate 38 , nitrate 39 , nitrite 40 and metal oxide 41 reduction, or transferred to a syntrophic partner via direct interspecies electron transfer (DIET) 42 . Similar to the iron metabolising Geoglobus 22,43,44 and Ferroglobus 45 within the Archaeoglobi, rG16 does not encode dsrAB , but was found to encode 10 multi-haem c-type cytochromes (MHCs) with 4 -31 haem binding motifs that may facilitate iron reduction 8,43,44,46 , or DIET as proposed in anaerobic methanotrophic archaea 42 . To compare the multi-haem cytochrome profile of rG16 with other Bacteria and Archaea, a network analysis was conducted on genomes from NCBI's RefSeq database.…”

“…Archaeoglobi is a class of thermophilic Archaea belonging to the Euryarchaeota that are abundant in subsurface hydrothermal environments, where they likely play a role in carbon and nutrient cycling 8,9 . The Archaeoglobi are split into three genera: Archaeoglobus , which are all heterotrophic or chemolithotrophic sulfate reducers [10][11][12][13][14][15][16][17][18][19] , and Geoglobus and Ferroglobus , which reduce both nitrate and ferric iron [20][21][22] . Pure cultures of Archaeoglobus have been shown to be capable of alkane oxidation 23,24 , and based on their shared metabolic features with methanogens [25][26][27][28] and proximity to methanogens in the genome tree, are suggested to have an ancestor capable of methanogenesis.…”