Abstract
Bacterial production of long-chain omega-3 polyunsaturated fatty acids (PUFAs), such as eicosapentaenoic acid (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n-3), is constrained to a narrow subset of marine γ-proteobacteria. The genes responsible for de novo bacterial PUFA biosynthesis, designated pfaEABCD, encode large, multi-domain protein complexes akin to type I iterative fatty acid and polyketide synthases, herein referred to as “Pfa synthases”. In addition to the archetypal Pfa synthase gene products from marine bacteria, we have identified homologous type I FAS/PKS gene clusters in diverse microbial lineages spanning 45 genera representing 10 phyla, presumed to be involved in long-chain fatty acid biosynthesis. In total, 20 distinct types of gene clusters were identified. Collectively, we propose the designation of “secondary lipids” to describe these biosynthetic pathways and products, a proposition consistent with the “secondary metabolite” vernacular. Phylogenomic analysis reveals a high degree of functional conservation within distinct biosynthetic pathways. Incongruence between secondary lipid synthase functional clades and taxonomic group membership combined with the lack of orthologous gene clusters in closely related strains suggests horizontal gene transfer has contributed to the dissemination of specialized lipid biosynthetic activities across disparate microbial lineages.
Highlights
Bacteria have evolved the capacity for fatty acid biosynthesis for incorporation into membrane phospholipids in three distinct ways
Additional analyses are presented to support the definition of secondary lipid synthases and differentiate these gene clusters from those involved in PKS or NRPS products based on phosphopantetheinyl transferase (PPTase) domain conservation
We analyze the ecology and physiological properties of these organisms to provide insight into possible traits unifying secondary lipid production potential and present evidence showing that horizontal gene transfer has aided in the dissemination of these biosynthetic gene clusters
Summary
Bacteria have evolved the capacity for fatty acid biosynthesis for incorporation into membrane phospholipids in three distinct ways. The most common mechanism is the prototypical type II Fatty Acid Synthase (FAS II), well characterized in E. coli [1]. In this system individual enzymatic activities reside on discrete enzyme products, encoded by the fatty acid biosynthesis, or fab, genes. FAS I consists of a large, multifunctional biosynthetic complex containing all enzymatic domains necessary for acyl chain elongation and functional derivatization and is responsible for the production of both membrane phospholipid fatty acyl chains as well as precursor fatty acid molecules for elongation to long-chain mycolic acids in members of the Corynebacteriaceae, Mycobacteriaceae and Nocardiaceae families [3]
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