Exploring photosynthesis evolution by comparative analysis of metabolic networks between chloroplasts and photosynthetic bacteria
1 Biomedical Instrument Institute, Shanghai Jiao Tong University, 1954 Huashan Rd, Shanghai, 200030, China
2 Department of Plant Biology, University of Illinois at Urbana-Champaign, 1201 W. Gregory Dr., Urbana, Illinois 61801, USA
3 The W. M. Keck Center for Comparative and Functional Genomics, University of Illinois at Urbana-Champaign, 1201 W. Gregory Dr., Urbana, Illinois 61801, USA
4 Shanghai Center for Bioinformation Technology, 100 Qinzhou Rd, 12th Floor, Shanghai, 200235, China
5 Department of Computer Engineering and Science, Shanghai University, 149 Yanchang Rd, Shanghai, 200072, China
BMC Genomics 2006, 7:100 doi:10.1186/1471-2164-7-100Published: 30 April 2006
Chloroplasts descended from cyanobacteria and have a drastically reduced genome following an endosymbiotic event. Many genes of the ancestral cyanobacterial genome have been transferred to the plant nuclear genome by horizontal gene transfer. However, a selective set of metabolism pathways is maintained in chloroplasts using both chloroplast genome encoded and nuclear genome encoded enzymes. As an organelle specialized for carrying out photosynthesis, does the chloroplast metabolic network have properties adapted for higher efficiency of photosynthesis? We compared metabolic network properties of chloroplasts and prokaryotic photosynthetic organisms, mostly cyanobacteria, based on metabolic maps derived from genome data to identify features of chloroplast network properties that are different from cyanobacteria and to analyze possible functional significance of those features.
The properties of the entire metabolic network and the sub-network that consists of reactions directly connected to the Calvin Cycle have been analyzed using hypergraph representation. Results showed that the whole metabolic networks in chloroplast and cyanobacteria both possess small-world network properties. Although the number of compounds and reactions in chloroplasts is less than that in cyanobacteria, the chloroplast's metabolic network has longer average path length, a larger diameter, and is Calvin Cycle -centered, indicating an overall less-dense network structure with specific and local high density areas in chloroplasts. Moreover, chloroplast metabolic network exhibits a better modular organization than cyanobacterial ones. Enzymes involved in the same metabolic processes tend to cluster into the same module in chloroplasts.
In summary, the differences in metabolic network properties may reflect the evolutionary changes during endosymbiosis that led to the improvement of the photosynthesis efficiency in higher plants. Our findings are consistent with the notion that since the light energy absorption, transfer and conversion is highly efficient even in photosynthetic bacteria, the further improvements in photosynthetic efficiency in higher plants may rely on changes in metabolic network properties.