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MBE Advance Access published online on June 15, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msi193
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Accepted June 10, 2005

Research Article

Evolutionary Implications of Bacterial Polyketide Synthases

Holger Jenke-Kodama 1, Axel Sandmann 2, Rolf Müller 2, and Elke Dittmann 1*

1 Humboldt University, Institute of Biology, Chausseestr. 117, 10115 Berlin
2 Pharmaceutical Biotechnology, Saarland University, P.O. Box 151150, 66041 Saarbrücken

* To whom correspondence should be addressed.
Elke Dittmann, E-mail: elke.dittmann{at}rz.hu-berlin.de


  Abstract

Polyketide synthases (PKS) perform a stepwise biosynthesis of diverse carbon skeletons from simple activated carboxylic acid units. The products of the complex pathways possess a wide range of pharmaceutical properties, including antibiotic, antitumor, antifungal and immunosuppressive activities. We have performed a comprehensive phylogenetic analysis of multimodular and iterative PKS of bacteria and fungi and of the distinct types of fatty acid synthases (FAS) from different groups of organisms based on the highly conserved ketoacyl synthase (KS) domains. Apart from enzymes that meet the classification standards we have included enzymes involved in the biosynthesis of mycolic acids, polyunsaturated fatty acids (PUFA) and glycolipids in bacteria. This study has revealed that PKS and FAS have passed through a long joint evolution process, in which modular PKS have a central position. They appear to have derived from bacterial FAS and primary iterative PKS, and in addition share a common ancestor with animal FAS and secondary iterative PKS. Furthermore, we have carried out a phylogenomic analysis of all modular PKS that are encoded by the complete eubacterial genomes currently available in the database. The phylogenetic distribution of acyl transferase (AT) and KS domain sequences revealed that multiple gene duplications, gene losses as well as horizontal gene transfer (HGT) have contributed to the evolution of PKS I in bacteria. The impact of these factors seems to vary considerably between the bacterial groups. Whereas in actinobacteria and cyanobacteria the majority of PKS I genes may have evolved from a common ancestor, several lines of evidence indicate that HGT has strongly contributed to the evolution of PKS I in proteobacteria. Discovery of new evolutionary links between PKS and FAS and between the different PKS pathways in bacteria may help us understanding the selective advantage that has led to the evolution of multiple secondary metabolite biosyntheses within individual bacteria.

Keywords: secondary metabolites; polyketides; multimodular enzymes; fatty acid synthases; Bayesian analysis.
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