Unexpected diversity of autotrophic carbon fixation pathways in Desulfovibrionales

Autotrophic CO₂ fixation is the most essential biosynthetic process and the basis of primary production. Today, seven pathways of inorganic carbon assimilation are known. This diversity of autotrophy represents the diversity of microorganisms and their ecological niches, whereas autotrophic pathways are often specific to particular taxonomic groups. The order Desulfovibrionales consists mainly of anaerobic sulfate-reducing bacteria, some of which are autotrophic. Our analysis of Pseudodesulfovibrio profundus (Desulfovibrionaceae) genome showed the presence of the genes for the key enzymes of the Calvin-Benson cycle. We were able to confirm that this bacterium is capable of growing autotrophically, while enzyme assays and proteomic analysis revealed that the bacterium does indeed use the Calvin-Benson cycle. A related Desulfovibrio desulfuricans (Desulfovibrionaceae) was shown to fix CO₂ via the recently described reductive glycine pathway [1]. Here, we found that the acetyl phosphate formed in this pathway is further metabolized via phosphate acetyltransferase and not through acetate kinase/acetyl-CoA synthetase reactions, as it was initially proposed based on proteomics data [1].

Furthermore, we found that halophilic Desulfovermiculus halophilus (Desulfohalobiaceae) uses the Wood-Ljundgdahl (WL) pathway for growth. We have further analyzed the efficiency of the autotrophic metabolism as a function of biomass production versus H₂S production and found the highest efficiency in D. desulfuricans, while P. profundus was the least efficient species. The efficiency of carbon fixation in D. halophilus using the WL pathway was lower than that of D. desulfuricans, probably due to the energetic costs of adaptation to halophilic conditions. Our analysis revealed considerable diversity of autotrophic metabolism in Desulfovibrionales. The evolution of autotrophic pathways in this bacterial group will be discussed.

[1] Sánchez-Andrea et al., Nat Comm 11:5090 (2020)