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EVOLUTION
The evolution of modularity in bacterial metabolic networks

Anat Kreimer^*, Elhanan Borenstein^,, Uri Gophna, and Eytan Ruppin^¶,||

*School of Mathematical Science, Department of Molecular Microbiology and Biotechnology, Faculty of Life Sciences, and ^¶School of Computer Science and School of Medicine, Tel Aviv University, Tel Aviv 69978, Israel; Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020; and Santa Fe Institute, Santa Fe, NM 87501

Edited by H. Eugene Stanley, Boston University, Boston, MA, and approved March 4, 2008 (received for review December 21, 2007)

Abstract

Deciphering the modular organization of metabolic networks and understanding how modularity evolves have attracted tremendous interest in recent years. Here, we present a comprehensive large scale characterization of modularity across the bacterial tree of life, systematically quantifying the modularity of the metabolic networks of >300 bacterial species. Three main determinants of metabolic network modularity are identified. First, network size is an important topological determinant of network modularity. Second, several environmental factors influence network modularity, with endosymbionts and mammal-specific pathogens having lower modularity scores than bacterial species that occupy a wider range of niches. Moreover, even among the pathogens, those that alternate between two distinct niches, such as insect and mammal, tend to have relatively high metabolic network modularity. Third, horizontal gene transfer is an important force that contributes significantly to metabolic modularity. We additionally reconstruct the metabolic network of ancestral bacterial species and examine the evolution of modularity across the tree of life. This reveals a trend of modularity decrease from ancestors to descendants that is likely the outcome of niche specialization and the incorporation of peripheral metabolic reactions.

horizontal gene transfer | lateral gene transfer | systems biology | bacterial evolution | network modules

Author contributions: A.K. and E.B. contributed equally to this work; A.K. and E.R. designed research; A.K. and E.B. performed research; A.K., E.B., and U.G. analyzed data; and A.K., E.B., U.G., and E.R. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

^||To whom correspondence should be addressed. E-mail: ruppin{at}post.tau.ac.il

© 2008 by The National Academy of Sciences of the USA

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