Five structural genes required for ceramide synthesis in Caulobacter and for bacterial survival

Abstract

Summary Sphingolipids are essential and common membrane components in eukaryotic organisms, participating in many important cellular functions. Only a few bacteria are thought to harbour sphingolipids in their membranes, among them the well‐studied α‐proteobacterium Caulobacter crescentus, a model organism for asymmetric cell division and cellular differentiation. Here, we report that C. crescentus wild type produces several molecular species of dihydroceramides, which are not produced in a mutant lacking the structural gene for serine palmitoyltransferase (spt). Whereas growth of a spt‐deficient mutant and wild type are indistinguishable during the exponential phase of growth, survival of the spt‐deficient mutant is much reduced, in comparison with wild type, during stationary phase of growth, especially at elevated temperatures. The structural gene for spt is located within a genomic cluster, comprising another 16 genes and which, like spt, are important for fitness of C. crescentus. Mutants deficient in genes linked to spt by high cofitness were unable to produce dihydroceramide or to survive in stationary phase of growth at elevated temperatures. At least five structural genes are required for dihydroceramide biosynthesis in C. crescentus and sphingolipid biosynthesis is needed for survival of this bacterium and the integrity of its outer membrane.

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“…Distribution of the four-genes spt operon as determined by detailed genomic searches (Supplementary Table S3). Note that Sphingomonadales, which are well known to produce ceramide lipids [27,28], are not represented because they have different variants of the operon with at least one of its genes displaced in other genomic regions [27,29].…”

“…The second approach we used in (Table 1) followed a conventional absence-presence analysis (Supplementary Table S3). We first conducted PSI-BLAST searches of putative homologs of Caulobacter SPT [27,29] in all the genomes of our in-house repository, plus those of closely related taxa. An Evalue cut-off of 5e -68 was generally sufficient to differentiate genuine SPT homologs from related α-oxo-amine synthases such as 5-aminolevulinate synthase.…”

“…Sphingolipids constitute a vast class of membrane lipids that are ubiquitous in eukaryotes, but scarcely present in bacteria [27,28]. To produce the precursor of ceramide, bacteria often require a four-genes operon ending with the gene for an α-oxoamine synthase catalyzing the key step of ceramide biosynthesis: serine palmitoyl-transferase (SPT) (Fig.…”

“…The second approach we used in (Table 1) followed a conventional absence-presence analysis (Supplementary Table S3). We first conducted PSI-BLAST searches of putative homologs of Caulobacter SPT [27,29] in all the genomes of our in-house repository, plus those of closely related taxa.…”

Natural Ligand-Mimetic and Nonmimetic Inhibitors of the Ceramide Transport Protein CERT

“…Sphingolipids are a class of lipids that contain the long-chain amino alcohols termed sphingoid bases, including sphingosine, dihydrosphingosine, and phytosphingosine, as their structural backbone (Figure 1A). Sphingolipids are ubiquitous constituents of cell membranes in eukaryotes and also present in a limited number of prokaryote species [11][12][13][14]. Sphingolipids participate in various biological events, including cell growth, apoptosis, differentiation, and adhesion (reviewed in [15,16]).…”