Chemical biology of Mycobacterium tuberculosis: deciphering the role of polyketide synthases in mycobacteria


 

Principal Investigator :  Rajesh S Gokhale

Project Associate/Assistant
Priti Saxena

Ph D Students
Omita Mehta
Yogyata

Collaborator
Debasisa Mohanty

This laboratory is interested in genome-based approaches to identify and exploit the microbial metabolic pathways that are involved in the biosynthesis of various natural products. The present focus is to understand the importance of various polyketide synthase gene clusters from Mycobacterium tuberculosis. The genome sequence of M.tuberculosis has revealed a remarkable array of genes that are homologous to polyketide synthases. Polyketide synthases (PKSs) are a class of enzymes that are involved in the biosynthesis of secondary metabolites such as erythromycin, rapamycin, tetracycline, lovastatin and resveratrol. Our study attempts to understand and exploit the role of polyketide synthases in the biology of M.tuberculosis. Previous studies with Actinomycetes PKS systems have shown that genes involved in the biosynthesis of a particular metabolite are clustered in one region of the genome. We have therefore decided to dedicate our initial efforts in studying two large PKS gene clusters that have been identified during the genome sequencing of M.tuberculosis.

A.  PKS gene cluster consisting of architecturally two different types of PKS proteins

This gene cluster contains six different open reading frames (ORFs). Our analysis suggested that there are architecturally at least two different types of PKS genes in this cluster. Four modular genes, pks7, pks8, pks17, and pks9 are flanked on either side by two chalcone synthase-like genes, pks10 and pks11. Such an unusual organization of the gene cluster has not been reported earlier. Further analyses of their domains suggested that pks7 is one complete module with all three reductive domains. pks8 in contrast is only a partial module, as the acyl carrier protein (ACP) domain is absent from this protein. Remarkably, pks17 complements by providing rest of the domains. pks9 gene is similar to several chain initiation modules, where active site cys residue of ketosynthase (KS) domain is mutated to gln (KSQ). Such modules have been implicated in decarboxylation of the starter units. Chalcone synthases have been traditionally studied from plant kingdom. These enzymes were recently characterized in Streptomyces as well.

Our approach for studying this PKS gene cluster is based on the expression of their cognate genes in S.coelicolor and E.coli. We have been able to produce pks10 and pks11 proteins in E.coli. These proteins were expressed as hexa-histidine fusion constructs and were purified to homogeneity using Ni-NTA affinity column. We are presently trying to decipher the substrate specificity of these proteins. It is known that chalcone synthase-like proteins use different acyl-coenzyme A as substrates, which results in the biosynthesis of diverse metabolic products. In order to predict the substrates for pks10 and pks11, we have initiated a structure-based modeling approach in collaboration with Dr. Mohanty’s group. The crystal structures of two chalcone synthase-like proteins and their complexes with several substrates and inhibitors are available in Protein Data Bank. By using homology modeling, we are trying to predict the structures along with their substrate specificity for the mycobacterial chalcone synthases

B.    Virulent gene cluster containing ppsA-E genes

The ppsA-E gene cluster consists of five modular PKS genes. These genes are a part of a large gene cluster spanning 50 kb of DNA, which putatively codes for 16 ORFs. These genes have been implicated in the biosynthesis of phthiocerol and phenolphthiocerol derivatives, a group of molecules restricted to eight mycobacterial species, seven of them being strict or opportunistic pathogens. This cluster consists of (1) PKS genes (ppsA-E), (2) the FAS gene mycocerosic acid synthase (mas), (3) several acyl-CoA synthases and (4) number of genes homologous to transporter proteins. We have carried out a detailed sequence analysis of pps genes to identify various domains and catalytic sites present in the modular PKS proteins. These analyses have identified a number of unique features of these modular PKS proteins. ppsA contains an additional acyl carrier protein (ACP) domain located at the N-terminus end of the protein. The C-terminal end of ppsE protein possesses a domain that is homologous to condensation domain of non-ribosomal polypeptide synthetase (NRPS) proteins. Such domains have not been typically characterized in a modular PKSs. Based on the modular logic of the polyketide biosynthesis, combined with detailed analysis of various domains present in a given module, we are trying to ascertain the structure of the polyketide product. In order to assist our predictions, we have constructed a library of sequences of KS and AT domains from different PKSs. On the basis of sequence homology, molecular modeling and available homologous crystal structures, we are attempting to predict the amino acid residues that play a crucial role in determining the substrate specificity.

We have cloned number of these genes in E.coli by shot-gun method. We are presently engineering suitable restriction sites for cloning and expressing these proteins in E.coli and Streptomyces expression vectors.

Publications

Reviews/Proceedings

1.   Gokhale RS and Tuteja D (2001) Biochemistry of polyketide synthases In: Biotechnology (Eds. Reid and Rehm), WILEY-VCH Verlag GmbH Germany, 10 (in press).