Abstract
BackgroundChloroplasts 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.ResultsThe 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.ConclusionIn 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.
Highlights
Chloroplasts descended from cyanobacteria and have a drastically reduced genome following an endosymbiotic event
The complete list of enzymes of chloroplasts, photosynthetic bacteria, E.coli, Arabidopsis thaliana and Cyanidioschyzon merolae are all listed in Additional file 1
By comparing the topological properties and features of metabolic networks between chloroplasts and photosynthetic bacteria, we showed that the chloroplast metabolic networks are reduced and simplified on one hand, but highly specialized and modular on the other
Summary
Chloroplasts descended from cyanobacteria and have a drastically reduced genome following an endosymbiotic event. The ancestral cyanobacterial genome was drastically reduced, and many genes were transferred to the nuclear genome [1,3]. The majority of the enzymes in chloroplast metabolic networks are nucleus-encoded, translated in cytosol, and imported into chloroplasts [4]. Such massive transportation of proteins requires a large amount of energy and sophisticated regulation from plant cells. Since the metabolic networks in chloroplasts are mostly constructed with proteins encoded in nuclear genome, do the networks exhibit some unique properties and characteristics that deviate from the ancestors' metabolic networks? Since the metabolic networks in chloroplasts are mostly constructed with proteins encoded in nuclear genome, do the networks exhibit some unique properties and characteristics that deviate from the ancestors' metabolic networks? To answer this question, we conducted a comparative study of the metabolic networks between chloroplasts and several photosynthetic bacteria
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