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PNAS 105 (21): 7500-7505

Copyright © 2008 by the National Academy of Sciences.


BIOLOGICAL SCIENCES / EVOLUTION

Modularity of stress response evolution

Amoolya H. Singh*,{dagger},{ddagger}, Denise M. Wolf{dagger},§, Peggy Wang*, and Adam P. Arkin*,{dagger},§

{dagger}Physical Biosciences Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, MS 9-144, Berkeley, CA 94720; *Department of Bioengineering, University of California, Berkeley, CA 94720; and §Virtual Institute for Microbial Stress and Survival, Lawrence Berkeley National Laboratory, Berkeley, CA 94720

Edited by Richard E. Lenski, Michigan State University, East Lansing, MI, and approved March 20, 2008

Received for publication October 14, 2007.

Abstract: Responses to extracellular stress directly confer survival fitness by means of complex regulatory networks. Despite their complexity, the networks must be evolvable because of changing ecological and environmental pressures. Although the regulatory networks underlying stress responses are characterized extensively, their mechanism of evolution remains poorly understood. Here, we examine the evolution of three candidate stress response networks (chemotaxis, competence for DNA uptake, and endospore formation) by analyzing their phylogenetic distribution across several hundred diverse bacterial and archaeal lineages. We report that genes in the chemotaxis and sporulation networks group into well defined evolutionary modules with distinct functions, phenotypes, and substitution rates as compared with control sets of randomly chosen genes. The evolutionary modules vary in both number and cohesiveness among the three pathways. Chemotaxis has five coherent modules whose distribution among species shows a clear pattern of interdependence and rewiring. Sporulation, by contrast, is nearly monolithic and seems to be inherited vertically, with three weak modules constituting early and late stages of the pathway. Competence does not seem to exhibit well defined modules either at or below the pathway level. Many of the detected modules are better understood in engineering terms than in protein functional terms, as we demonstrate using a control-based ontology that classifies gene function according to roles such as "sensor," "regulator," and "actuator." Moreover, we show that combinations of the modules predict phenotype, yet surprisingly do not necessarily correlate with phylogenetic inheritance. The architectures of these three pathways are therefore emblematic of different modes and constraints on evolution.

Key Words: chemotaxis • competence • module • regulatory • sporulation


Author contributions: A.H.S., D.M.W., and A.P.A. designed research; A.H.S. and P.W. performed research; A.H.S. and D.M.W. contributed new reagents/analytic tools; A.H.S. and D.M.W. analyzed data; and A.H.S., D.M.W., and A.P.A. wrote the paper.

{ddagger}Present address: European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0709764105/DCSupplemental.

To whom correspondence may be addressed. E-mail: aparkin{at}lbl.gov or dmwolf{at}lbl.gov

© 2008 by The National Academy of Sciences of the USA


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