The Complete Genome Sequence of Thermococcus onnurineus NA1 Reveals a Mixed Heterotrophic and Carboxydotrophic Metabolism

Abstract

Members of the genus Thermococcus, sulfur-reducing hyperthermophilic archaea, are ubiquitously present in various deep-sea hydrothermal vent systems and are considered to play a significant role in the microbial consortia. We present the complete genome sequence and feature analysis of Thermococcus onnurineus NA1 isolated from a deep-sea hydrothermal vent area, which reveal clues to its physiology. Based on results of genomic analysis, T. onnurineus NA1 possesses the metabolic pathways for organotrophic growth on peptides, amino acids, or sugars. More interesting was the discovery that the genome encoded unique proteins that are involved in carboxydotrophy to generate energy by oxidation of CO to CO 2 , thereby providing a mechanistic basis for growth with CO as a substrate. This lithotrophic feature in combination with carbon fixation via RuBisCO (ribulose 1,5-bisphosphate carboxylase/oxygenase) introduces a new strategy with a complementing energy supply for T. onnurineus NA1 potentially allowing it to cope with nutrient stress in the surrounding of hydrothermal vents, providing the first genomic evidence for the carboxydotrophy in Thermococcus.Deep-sea hydrothermal vents comprise a plethora of potential habitats, with gradients of nutrient and extreme physicochemical conditions that vary from high to low with respect to temperature (350 to 2°C), oxygenation states, and fluid velocities (13). Many multidisciplinary studies have been carried out to understand the complexities of hydrothermal vent systems. Biological studies have also been accomplished using samples collected from hydrothermal vent areas and culture-dependent and culture-independent techniques, revealing the presence of physiologically, metabolically, and phylogenetically diverse microorganisms (15). These findings have been followed by characterization of many bacterial and archaeal thermophiles (and hyperthermophiles), including both chemolithoautotrophic and chemoorganoheterotrophic strains. Among representative species of the Archaea, sulfur-reducing heterotrophs belonging to the order Thermococcales (encompassing the genera Thermococcus, Pyrococcus, and Palaeococcus) have been reported to be one of the predominant groups (20, 25). Notably, members of the species of Thermococcus were found to be more abundant in the vent ecosystem, with such isolates more frequently reported than the Pyrococcus species (9,11,23,24). Such large populations indicate some significance for the presence of Thermococcus in the microbial consortia that make up the microbial ecology of hydrothermal vent systems.In addition to ecological significance, the hyperthermophilic feature of Thermococcales has fascinated microbiologists interested in fundamental and/or application-based research. To date, the complete genome sequences of three Pyrococcus species, i.e., Pyrococcus horikoshii (16), Pyrococcus furiosus (26), and Pyrococcus abyssi (5), and a Thermococcus strain, Thermococcus kodakaraensis KOD1 (7), have been determined. Analysis of the sequences and the physiolo...

A thermophilic, hydrogenogenic and carboxydotrophic bacterium, Calderihabitans maritimus gen. nov., sp. nov., from a marine sediment core of an undersea caldera

“…Thermococcus strain AM4 was the first hydrogenogenic, carboxydotrophic archaeon isolated from a deep-sea hydrothermal vent (Sokolova et al, 2004). Culture-based study has shown the inability of many other strains representing the genus Thermococcus to consume CO, although genomic studies revealed that 'Thermococcus onnurineus' (Lee et al, 2008), Thermococcus barophilus (Vannier et al, 2011) and AM4 ECH gene sets by lateral gene transfer among strains of the genus Thermococcus. Thus, CO oxidation in the thermococci seems neither a major component of metabolism nor common trait in the genus.…”

Distinct Physiological Roles of the Three [NiFe]-Hydrogenase Orthologs in the Hyperthermophilic Archaeon Thermococcus kodakarensis

“…The three types of [NiFe]-hydrogenase orthologs (Hyh, Mbh, and Mbx) found in P. furiosus are commonly distributed in the other completely sequenced genomes of Thermococcales, i.e., Pyrococcus horikoshii (16), Pyrococcus abyssi (4), Thermococcus kodakarensis (8), Thermococcus onnurineus (22), Thermococcus sibiricus (30), and Thermococcus gammatolerans (52). Mbh and Mbx orthologs are present in all species; Hyh orthologs are also found in all species, with the exception of T. gammatolerans.…”

Characterization of a Zinc-Containing Alcohol Dehydrogenase with Stereoselectivity from the Hyperthermophilic Archaeon Thermococcus guaymasensis

“…All members of the genus Thermococcus are chemoorganotrophs which can grow on peptide-containing substrates (6,50), and some of them are able to utilize carbohydrates, including starch and chitin as a carbon source (6), though some are capable of producing H 2 from CO (38,61). Glycolysis from glucose to pyruvate in Thermococcus celer and Thermococcus litoralis appears to occur via a modified Embden-Meyerhof (EM) pathway containing ADP-dependent hexose kinase and phosphofructokinase and a tungsten-containing glyceraldehyde-3-phosphate, ferredoxin oxidoreductase (59).…”