Phylogenomic reconstruction of archaeal fatty acid metabolism

Abstract

While certain archaea appear to synthesize and/or metabolize fatty acids, the respective pathways still remain obscure. By analyzing the genomic distribution of the key lipid-related enzymes, we were able to identify the likely components of the archaeal pathway of fatty acid metabolism, namely, a combination of the enzymes of bacterial-type β-oxidation of fatty acids (acyl-CoA-dehydrogenase, enoyl-CoA hydratase, and 3-hydroxyacyl-CoA dehydrogenase) with paralogs of the archaeal acetyl-CoA C-acetyltransferase, an enzyme of the mevalonate biosynthesis pathway. These three β-oxidation enzymes working in the reverse direction could potentially catalyze biosynthesis of fatty acids, with paralogs of acetyl-CoA C-acetyltransferase performing addition of C2 fragments. The presence in archaea of the genes for energy-transducing membrane enzyme complexes, such as cytochrome bc complex, cytochrome c oxidase, and diverse rhodopsins, was found to correlate with the presence of the proposed system of fatty acid biosynthesis. We speculate that because these membrane complexes functionally depend on fatty acid chains, their genes could have been acquired via lateral gene transfer from bacteria only by those archaea that already possessed a system of fatty acid biosynthesis. The proposed pathway of archaeal fatty acid metabolism operates in extreme conditions and therefore might be of interest in the context of biofuel production and other industrial applications.

Emergence of cytochrome bc complexes in the context of photosynthesis

“…More bulky isoprenoid tails of archaeal lipids not always could substitute for fatty acid chains, so that fatty acids that are found within archaeal membrane enzymes (Kolbe et al ), most likely, indicate their bacterial origin. The archaeal hosts of such enzymes, while lacking full‐fledged fatty acid synthases, appear to be able to synthesize fatty acids, to stabilize their membrane enzymes of bacterial origin, by combing bacterial‐type enzymes of beta‐oxidation of fatty acids – working in the reverse mode – with archaea‐specific acetyl‐CoA C‐acetyltransferase (Dibrova et al ). Therefore, the presence of these enzymes may serve as an indication of the presence of membrane enzymes of bacterial origin in the particular archaea (Dibrova et al ).…”

“…The archaeal hosts of such enzymes, while lacking full‐fledged fatty acid synthases, appear to be able to synthesize fatty acids, to stabilize their membrane enzymes of bacterial origin, by combing bacterial‐type enzymes of beta‐oxidation of fatty acids – working in the reverse mode – with archaea‐specific acetyl‐CoA C‐acetyltransferase (Dibrova et al ). Therefore, the presence of these enzymes may serve as an indication of the presence of membrane enzymes of bacterial origin in the particular archaea (Dibrova et al ). As shown in Table S1 in archaea, the presence of the genes that encode the enzymes of fatty acid metabolism strictly correlates with the presence of genes of cyt bc complexes.…”

Structure and Evolution of the Archaeal Lipid Synthesis Enzyme sn-Glycerol-1-phosphate Dehydrogenase

“…Biochemical and phylogenomic analyses have suggested that isoprenoids and fatty acid synthesis genes might have been present in the LUCA (10,50,64). However, a recent extensive phylogenomic analysis of the presence of fatty acid synthesis genes in Archaea contradicts the latter suggestion, instead indicating that in those archaea containing fatty acid synthesis genes (a chimeric pathway with both bacterial-like and archaeal genes) most of the genes were likely acquired from bacteria (65). Gene distributions across the archaeal-bacterial divide can reflect either presence in the LUCA or later origins followed by interdomain lateral gene transfer (66,67) whereby distinctions between the two are not always easy.…”

Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics

“…In bacterial lipids, the hydrophobic tails are routinely linked to the glycerol moiety by ester bonds whereas archaeal lipids contain ether bonds. The difference extends beyond the chemical structures of the phospholipids, to the evolutionary provenance of the enzymes involved in synthesis of phospholipids: most of these are either non-homologous or distantly related, but not orthologous, in bacteria and archaea [70–74]. The only lipid biosynthetic pathways common for bacteria and archaea are the mevalonate pathway of isoprenoid biosynthesis and the enzymatic machinery for attaching polar heads to the protruding phosphate groups of lipid biosynthesis intermediates [70, 74, 75].…”