Abstract
BackgroundA central tenet in biochemistry for over 50 years has held that microorganisms, plants and, more recently, certain apicomplexan parasites synthesize essential aromatic compounds via elaboration of a complete shikimic acid pathway, whereas metazoans lacking this pathway require a dietary source of these compounds. The large number of sequenced bacterial and archaean genomes now available for comparative genomic analyses allows the fundamentals of this contention to be tested in prokaryotes. Using Hidden Markov Model profiles (HMM profiles) to identify all known enzymes of the pathway, we report the presence of genes encoding shikimate pathway enzymes in the hypothetical proteomes constructed from the genomes of 488 sequenced prokaryotes.ResultsAmongst free-living prokaryotes most Bacteria possess, as expected, genes encoding a complete shikimic acid pathway, whereas of the culturable Archaea, only one was found to have a complete complement of recognisable enzymes in its predicted proteome. It may be that in the Archaea, the primary amino-acid sequences of enzymes of the pathway are highly divergent and so are not detected by HMM profiles. Alternatively, structurally unrelated (non-orthologous) proteins might be performing the same biochemical functions as those encoding recognized genes of the shikimate pathway. Most surprisingly, 30% of host-associated (mutualistic, commensal and pathogenic) bacteria likewise do not possess a complete shikimic acid pathway. Many of these microbes show some degree of genome reduction, suggesting that these host-associated bacteria might sequester essential aromatic compounds from a parasitised host, as a 'shared metabolic adaptation' in mutualistic symbiosis, or obtain them from other consorts having the complete biosynthetic pathway. The HMM results gave 84% agreement when compared against data in the highly curated BioCyc reference database of genomes and metabolic pathways.ConclusionsThese results challenge the conventional belief that the shikimic acid pathway is universal and essential in prokaryotes. The possibilities that non-orthologous enzymes catalyse reactions in this pathway (especially in the Archaea), or that there exist specific uptake mechanisms for the acquisition of shikimate intermediates or essential pathway products, warrant further examination to better understand the precise metabolic attributes of host-beneficial and pathogenic bacteria.
Highlights
A central tenet in biochemistry for over 50 years has held that microorganisms, plants and, more recently, certain apicomplexan parasites synthesize essential aromatic compounds via elaboration of a complete shikimic acid pathway, whereas metazoans lacking this pathway require a dietary source of these compounds
Bioinformatic analyses established that horizontal transfer of ancestral genes of the shikimic acid pathway into the N. vectensis genome occurred from both bacteria and algae
We interrogate the hypothetical proteomes of prokaryotes, constructed from their published genomes, to profile the universality of the shikimic acid pathway with a view to understanding a key metabolic process of freeliving and host-associated bacteria
Summary
A central tenet in biochemistry for over 50 years has held that microorganisms, plants and, more recently, certain apicomplexan parasites synthesize essential aromatic compounds via elaboration of a complete shikimic acid pathway, whereas metazoans lacking this pathway require a dietary source of these compounds. For genes to be missing from an essential biosynthetic pathway might be accounted for by the presence of genes having low sequence similarity to the known genes, or substitution by alternative enzymes having an analogous function. Another possibility is that steps of a biosynthetic pathway may be bypassed if substrates and endproducts are readily obtained from the surrounding environment [5]. The recent surge in microbial genome sequencing has produced a wealth of genetic data available for comparative genomic analyses to make possible the identification of diverse essential enzymes in critical metabolic pathways within the Archaea and Bacteria. We interrogate the hypothetical proteomes of prokaryotes, constructed from their published genomes, to profile the universality of the shikimic acid pathway with a view to understanding a key metabolic process of freeliving and host-associated bacteria
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