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A global analysis of adaptive evolution of operons in cyanobacteria

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Abstract

Operons are an important feature of prokaryotic genomes. Evolution of operons is hypothesized to be adaptive and has contributed significantly towards coordinated optimization of functions. Two conflicting theories, based on (i) in situ formation to achieve co-regulation and (ii) horizontal gene transfer of functionally linked gene clusters, are generally considered to explain why and how operons have evolved. Furthermore, effects of operon evolution on genomic traits such as intergenic spacing, operon size and co-regulation are relatively less explored. Based on the conservation level in a set of diverse prokaryotes, we categorize the operonic gene pair associations and in turn the operons as ancient and recently formed. This allowed us to perform a detailed analysis of operonic structure in cyanobacteria, a morphologically and physiologically diverse group of photoautotrophs. Clustering based on operon conservation showed significant similarity with the 16S rRNA-based phylogeny, which groups the cyanobacterial strains into three clades. Clade C, dominated by strains that are believed to have undergone genome reduction, shows a larger fraction of operonic genes that are tightly packed in larger sized operons. Ancient operons are in general larger, more tightly packed, better optimized for co-regulation and part of key cellular processes. A sub-clade within Clade B, which includes Synechocystis sp. PCC 6803, shows a reverse trend in intergenic spacing. Our results suggest that while in situ formation and vertical descent may be a dominant mechanism of operon evolution in cyanobacteria, optimization of intergenic spacing and co-regulation are part of an ongoing process in the life-cycle of operons.

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Acknowledgments

This work was partially supported by a grant from Department of Biotechnology, Government of India awarded to PPW and funding from the Consortium for Clean Coal Utilization at Washington University to PPW and HBP. DM was supported by the DBT-BINC-JRF Program. Part of the work was carried out with support from M.Sc.-DBT-Studentship availed by DM at the Bioinformatics Centre, University of Pune. The authors acknowledge useful discussions with Dr. Urmila Kulkarni-Kale of University of Pune. The authors thank Kruti Nandu for help with microarray data normalization, Dilip A. Durai for the development of cyano-operon database and anonymous reviewers for constructive comments.

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  1. Danish Memon

    Present address: Cancer Research UK Applied Computational Biology and Bioinformatics Group, Paterson Institute for Cancer Research, The University of Manchester, Christie Hospital Site, Manchester, M20 4BX, UK

Authors and Affiliations

  1. Department of Chemical Engineering, Indian Institute of Technology Bombay, Powai, Mumbai, 400076, India

    Danish Memon & Pramod P. Wangikar

  2. Bioinformatics Centre, University of Pune, Pune, 411007, India

    Danish Memon

  3. Department of Biology, Washington University, St. Louis, MO, 63130, USA

    Abhay K. Singh & Himadri B. Pakrasi

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Memon, D., Singh, A.K., Pakrasi, H.B. et al. A global analysis of adaptive evolution of operons in cyanobacteria. Antonie van Leeuwenhoek 103, 331–346 (2013). https://doi.org/10.1007/s10482-012-9813-0

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