Study of the distribution of autotrophic CO2 fixation cycles in Crenarchaeota

Abstract

Two new autotrophic carbon fixation cycles have been recently described in Crenarchaeota. The 3-hydroxypropionate/4-hydroxybutyrate cycle using acetyl-coenzyme A (CoA)/propionyl-CoA carboxylase as the carboxylating enzyme has been identified for (micro)aerobic members of the Sulfolobales. The dicarboxylate/4-hydroxybutyrate cycle using oxygen-sensitive pyruvate synthase and phosphoenolpyruvate carboxylase as carboxylating enzymes has been found in members of the anaerobic Desulfurococcales and Thermoproteales. However, Sulfolobales include anaerobic and Desulfurococcales aerobic autotrophic representatives, raising the question of which of the two cycles they use. We studied the mechanisms of autotrophic CO 2 fixation in the strictly anaerobic Stygiolobus azoricus (Sulfolobales) and in the facultatively aerobic Pyrolobus fumarii (Desulfurococcales). The activities of all enzymes of the 3-hydroxypropionate/4-hydroxybutyrate cycle were found in the anaerobic S. azoricus. In contrast, the aerobic or denitrifying P. fumarii possesses all enzyme activities of the dicarboxylate/4-hydroxybutyrate cycle. We conclude that autotrophic Crenarchaeota use one of the two cycles, and that their distribution correlates with the 16S rRNA-based phylogeny of this group, rather than with the aerobic or anaerobic lifestyle.

Carboxylases in Natural and Synthetic Microbial Pathways

“…On the other hand-and in line with the oxygen sensitivity of its ferredoxindependent carboxylase-the DC/HB cycle seems to be limited to anaerobic autotrophic species of the Thermoproteales and Desulfurococcales order (18,64,102). In contrast, the HP/HB cycle was found to operate in (micro)aerobic members of the Sulfolobales order, as well as in aerobic marine group I archaea ("Taumarchaeota") (16,18,19).…”

Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO 2 fixation

“…Genomic studies of the Thaumarchaeota suggested a functioning HP/HB cycle (4,13,(19)(20)(21)(22), which was first identified in the thermophilic crenarchaeon Metallosphaera sedula (19) and was extended to other aerobic Crenarchaeota (14,23). Briefly, one acetyl-CoA and two bicarbonate molecules are converted via 3-hydroxypropionate to succinyl-CoA.…”

Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat

“…All six carbon fixation pathways known to date (Berg et al, 2010) were incomplete or undetectable in Fn1 (Supplementary Figure S5a). This latter feature is distinct from other sequenced thaumarchaeal and autotrophic crenarchaeal genomes (Berg et al, 2010;Beam et al, 2014;Konneke et al, 2014), further building on previous evidence which suggests a more versatile metabolism for members of the Phylum Thaumarchaeota (for example, bacterial ectosymbionts (Muller et al, 2010) and facultative ammonia oxidizers (Mussmann et al, 2011)). Fn1 is not predicted to ferment pyruvate to end products such as acetate, butyrate, ethanol, H 2 , lactate, and propionate (Supplementary Table S3).…”