The Genome Sequence of the Crenarchaeon
            <i>Acidilobus saccharovorans</i>
            Supports a New Order,
            <i>Acidilobales</i>
            , and Suggests an Important Ecological Role in Terrestrial Acidic Hot Springs

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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 ...

Section: Resultsmentioning

confidence: 99%

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

Mardanov

Slododkina

Slobodkin

et al. 2015

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“…Such a hypothesis is consistent with the two po-tential models for S 8 0 reduction proposed for the closely related strain Acidilobus saccharovorans based on genomic data. Here, either a soluble cytoplasmic NAD(P)H-elemental sulfur oxidoreductase (ASAC_1028) or a cytoplasmic membrane-bound sulfur-reducing complex (ASAC_1394-ASA_1397) functions to reduce S 8 0 using reduced NAD(P)H or quinones as the electron donor (51). Importantly, biochemical evidence confirming these functions has yet to be documented in sulfur-reducing crenarchaeota.…”

Section: Discussionmentioning

confidence: 99%

Involvement of Intermediate Sulfur Species in Biological Reduction of Elemental Sulfur under Acidic, Hydrothermal Conditions

Boyd

Druschel

2013

The thermoacidophile and obligate elemental sulfur (S 8 0 )-reducing anaerobe Acidilobus sulfurireducens 18D70 does not associate with bulk solid-phase sulfur during S 8 0 -dependent batch culture growth. Cyclic voltammetry indicated the production of hydrogen sulfide (H 2 S) as well as polysulfides after 1 day of batch growth of the organism at pH 3.0 and 81°C. The production of polysulfide is likely due to the abiotic reaction between S 8 0 and the biologically produced H 2 S, as evinced by a rapid cessation of polysulfide formation when the growth temperature was decreased, inhibiting the biological production of sulfide. After an additional 5 days of growth, nanoparticulate S 8 0 was detected in the cultivation medium, a result of the hydrolysis of polysulfides in acidic medium. To examine whether soluble polysulfides and/or nanoparticulate S 8 0 can serve as terminal electron acceptors (TEA) supporting the growth of A. sulfurireducens, total sulfide concentration and cell density were monitored in batch cultures with S 8 0 provided as a solid phase in the medium or with S 8 0 sequestered in dialysis tubing. The rates of sulfide production in 7-day-old cultures with S 8 0 sequestered in dialysis tubing with pore sizes of 12 to 14 kDa and 6 to 8 kDa were 55% and 22%, respectively, of that of cultures with S 8 0 provided as a solid phase in the medium. These results indicate that the TEA existed in a range of particle sizes that affected its ability to diffuse through dialysis tubing of different pore sizes. Dynamic light scattering revealed that S 8 0 particles generated through polysulfide rapidly grew in size, a rate which was influenced by the pH of the medium and the presence of organic carbon. Thus, S 8 0 particles formed through abiological hydrolysis of polysulfide under acidic conditions appeared to serve as a growth-promoting TEA for A. sulfurireducens.

“…Nearly all cultivated representatives of this phylum can generate energy through the oxidation and/or fermentation of complex organic compounds (e.g., yeast extract or peptone), and this is often coupled with the reduction of elemental sulfur (8)(9)(10). With the exception of Acidilobus saccharovorans (11), other sequenced Desulfurococcales are too unrelated to those present in YNP to be of significant value for an understanding of community function (i.e., Aeropyrum pernix K1 [12], Desulfurococcus kamchatkensis [13], Hyperthermus butylicus [14], Ignicoccus hospitalis [15], and Staphylothermus marinus [16]). However, misannotation of specific genes within Ac.…”

mentioning

confidence: 99%

“…Furthermore, previous suggestions that Caldisphaera and Acidilobus spp. comprised a new order (Acidilobales) within the class Thermoprotei (Crenarchaeota) (8,11,17) have been clarified, and phylogenetic analyses indicate that these organisms belong within the Desulfurococcales (18). Common genomic and physiological attributes of sequenced members of the Desulfurococcales include pathways for catabolism and anabolism of complex carbon sources, including both proteins and carbohydrates.…”

mentioning

confidence: 99%

Predominant Acidilobus-Like Populations from Geothermal Environments in Yellowstone National Park Exhibit Similar Metabolic Potential in Different Hypoxic Microbial Communities

Jay

Rusch

Tringe

et al. 2014

c High-temperature (>70°C) ecosystems in Yellowstone National Park (YNP) provide an unparalleled opportunity to study chemotrophic archaea and their role in microbial community structure and function under highly constrained geochemical conditions. Acidilobus spp. (order Desulfurococcales) comprise one of the dominant phylotypes in hypoxic geothermal sulfur sediment and Fe(III)-oxide environments along with members of the Thermoproteales and Sulfolobales. Consequently, the primary goals of the current study were to analyze and compare replicate de novo sequence assemblies of Acidilobus-like populations from four different mildly acidic (pH 3.3 to 6.1) high-temperature (72°C to 82°C) environments and to identify metabolic pathways and/or protein-encoding genes that provide a detailed foundation of the potential functional role of these populations in situ. De novo assemblies of the highly similar Acidilobus-like populations (>99% 16S rRNA gene identity) represent near-complete consensus genomes based on an inventory of single-copy genes, deduced metabolic potential, and assembly statistics generated across sites. Functional analysis of coding sequences and confirmation of gene transcription by Acidilobus-like populations provide evidence that they are primarily chemoorganoheterotrophs, generating acetyl coenzyme A (acetyl-CoA) via the degradation of carbohydrates, lipids, and proteins, and auxotrophic with respect to several external vitamins, cofactors, and metabolites. No obvious pathways or protein-encoding genes responsible for the dissimilatory reduction of sulfur were identified. The presence of a formate dehydrogenase (Fdh) and other protein-encoding genes involved in mixed-acid fermentation supports the hypothesis that Acidilobus spp. function as degraders of complex organic constituents in high-temperature, mildly acidic, hypoxic geothermal systems. Microbial communities in high-temperature geothermal environments provide unique opportunities for determining the physiology of specific populations and for studying geobiological interactions central to a comprehensive functional and evolutionary understanding of thermophilic microorganisms. Acidic, hyperthermal (Ͼ70°C) systems from Yellowstone National Park (YNP) contain significant concentrations of reduced constituents such as H 2 , H 2 S, elemental sulfur, As(III) (e.g., H 3 AsO 3 ), Fe(II), and organic carbon (1, 2), which are often used as electron donors for different chemotrophic microorganisms (3). The oxidation of reduced compounds is coupled with the reduction of terminal electron acceptors, including O 2 , Fe(III), and different sulfur species, generating energy for cellular processes (3, 4). Thermophilic organisms catalyze reactions of geochemical significance (e.g., oxidation-reduction, biomineralization, acidification, and mineral dissolution) that are often orders of magnitude faster than the corresponding abiotic mechanisms (4-7).High-temperature acidic geothermal systems contain several predominant archaeal populations within the phylum Cr...