Summary auto-generated
This study investigates autotrophic CO2 fixation pathways in two unusual Crenarchaeota species. Crenarchaeota typically use one of two recently discovered CO2 fixation cycles: the 3-hydroxypropionate/4-hydroxybutyrate cycle (found in microaerophilic Sulfolobales) or the dicarboxylate/4-hydroxybutyrate cycle (found in anaerobic Desulfurococcales and Thermoproteales). However, some Sulfolobales are strictly anaerobic, and some Desulfurococcales are aerobic, raising questions about cycle usage. Researchers examined Stygiolobus azoricus (strictly anaerobic Sulfolobales) and Pyrolobus fumarii (facultatively aerobic Desulfurococcales) by measuring enzyme activities in cell extracts. S. azoricus possessed all enzyme activities for the 3-hydroxypropionate/4-hydroxybutyrate cycle, including biotin-dependent carboxylases. P. fumarii possessed all enzyme activities for the dicarboxylate/4-hydroxybutyrate cycle, lacking biotin-dependent carboxylases. The distribution of these two pathways correlates with phylogenetic relationships based on 16S rRNA sequences rather than lifestyle (aerobic versus anaerobic). High-temperature environments apparently protect sensitive enzymes like pyruvate synthase from oxygen inactivation in P. fumarii.
Key findings
- Strictly anaerobic S. azoricus uses the 3-hydroxypropionate/4-hydroxybutyrate CO2 fixation cycle characteristic of Sulfolobales, evidenced by detected biotin-dependent carboxylase activity
- Facultatively aerobic P. fumarii uses the dicarboxylate/4-hydroxybutyrate cycle characteristic of Desulfurococcales, lacking biotin-dependent carboxylases
- Crenarchaeota pathway distribution follows 16S rRNA-based phylogenetic classification rather than aerobic or anaerobic lifestyle
- Oxygen-sensitive pyruvate synthase and other dicarboxylate cycle enzymes remain functional in P. fumarii due to protection from high-temperature cellular environments
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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 CO2 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.