The Geoglobus acetivorans Genome: Fe(III) Reduction, Acetate Utilization, Autotrophic Growth, and Degradation of Aromatic Compounds in a Hyperthermophilic Archaeon

Abstract

bGeoglobus acetivorans is a hyperthermophilic anaerobic euryarchaeon of the order Archaeoglobales isolated from deep-sea hydrothermal vents. A unique physiological feature of the members of the genus Geoglobus is their obligate dependence on Fe(III) reduction, which plays an important role in the geochemistry of hydrothermal systems. The features of this organism and its complete 1,860,815-bp genome sequence are described in this report. Genome analysis revealed pathways enabling oxidation of molecular hydrogen, proteinaceous substrates, fatty acids, aromatic compounds, n-alkanes, and organic acids, including acetate, through anaerobic respiration linked to Fe(III) reduction. Consistent with the inability of G. acetivorans to grow on carbohydrates, the modified Embden-Meyerhof pathway encoded by the genome is incomplete. Autotrophic CO 2 fixation is enabled by the Wood-Ljungdahl pathway. Reduction of insoluble poorly crystalline Fe(III) oxide depends on the transfer of electrons from the quinone pool to multiheme c-type cytochromes exposed on the cell surface. Direct contact of the cells and Fe(III) oxide particles could be facilitated by pilus-like appendages. Genome analysis indicated the presence of metabolic pathways for anaerobic degradation of aromatic compounds and n-alkanes, although an ability of G. acetivorans to grow on these substrates was not observed in laboratory experiments. Overall, our results suggest that Geoglobus species could play an important role in microbial communities of deep-sea hydrothermal vents as lithoautotrophic producers. An additional role as decomposers would close the biogeochemical cycle of carbon through complete mineralization of various organic compounds via Fe(III) respiration. G eoglobus acetivorans SBH6T is a hyperthermophilic anaerobic euryarchaeon isolated from one of the world's deepest deepsea hydrothermal vents (Ashadze field; depth, 4,100 m) located on the Mid-Atlantic Ridge (1). A unique physiological feature of the members of the genus Geoglobus, which so far comprises only two species-G. ahangari and G. acetivorans-is their obligate dependence on Fe(III) reduction (1, 2). These microorganisms grow exclusively by coupling the oxidation of molecular hydrogen or organic compounds to the reduction of insoluble poorly crystalline Fe(III) oxide (ferrihydrite) or Fe(III) citrate. G. acetivorans can grow lithoautotrophically using CO 2 as a carbon source. G. acetivorans cannot use other electron acceptors such as sulfate, thiosulfate, elemental sulfur, nitrite, or oxygen for growth, and it is also unable to ferment organic compounds. Thus, these physiological features make G. acetivorans the ideal candidate for studies of the genomic and biochemical aspects of iron reduction.Microbial reduction of ferric iron plays an important role in the biogeochemical cycles of carbon, oxygen, and sulfur in the biosphere and has a considerable impact on the ecological situation in the modern environments (3). A more significant role may have been played by the reduction of iron in ...

Mechanisms Involved in Fe(III) Respiration by the Hyperthermophilic Archaeon Ferroglobus placidus

“…Direct contact with Fe(III) oxides and reliance on electron-shuttling or chelating compounds for reduction of Fe(III) are traits seen in both bacterial and archaeal species (1,(11)(12)(13)(14)(15)(16)61). In fact, the majority of electron transport proteins that transcriptomic and proteomic studies showed to be important for reduction of insoluble Fe(III) oxide by F. placidus have homologues in mesophilic Fe(III)-reducing bacteria.…”

“…F. placidus also is unique among the Archaeoglobaceae in that it can transfer electrons from the oxidation of aromatic compounds to Fe(III) (22)(23)(24). Although genes involved in aromatics degradation were identified in the G. acetivorans genome, attempts to grow G. acetivorans on such compounds have been unsuccessful (15). Therefore, any information regarding Fe(III) reduction by an aromatics-degrading hyperthermophile such as F. placidus is significant.…”

“…For example, Pyrobaculum aerophilum seems to release an electron-shuttling compound(s) that transfers electrons from the cell surface to the surface of Fe(III) oxides not in direct contact with the cells (13), while Geoglobus ahangari and Geoglobus acetivorans require direct contact with Fe(III) hydroxides in the absence of chelated iron or reduced electron shuttles (14,15). The involvement of c-type cytochrome proteins in Fe(III) reduction also seems to vary among hyperthermophilic archaea.…”

Enzymes of the benzoyl‐coenzyme A degradation pathway in the hyperthermophilic archaeon Ferroglobus placidus

“…Very recently, genes encoding putative enzymes involved in aromatic compound degradation similar to those in F. placidus were identified in the genome of the hyperthermophilic Geoglobus acetivorans, also belonging to the Archaeoglobales (Mardanov et al, 2015). Based on the genomic and transcriptomic analyses with F. placidus , the genes were assigned to code for enzymes of a Rhodopseudomonastype benzoyl-CoA degradation pathway.…”

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

“…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.…”