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Escherichia coli

Mechanisms of diversification and speciation during 40.000 generations of experimental evolution in Escherichia coli



The main goal of this project is to understand how bacterial diversity is generated and maintained, and to improve the knowledge about the dynamics of phenotypic and genomic evolution. This knowledge is crucial for better understanding the emergence and evolution of pathogens because many of the difficulties encountered during efforts to prevent and control infections are due to the potential of bacteria to generate extensive variability within populations (e.g. antibiotic resistance).

This genome sequencing project makes use of evolving strains that have been isolated from the longest-running evolution experiment using Escherichia coli. A clone of E. coli B was used as the common ancestor to found twelve independent populations (Lenski, 2004). These populations have been propagated by daily serial transfer in the same defined glucose-limited environment for more than 40.000 generations (Lenski et al., 1991; Lenski and Travisano, 1994; Cooper and Lenski, 2000; Philippe et al., 2007). Over time, the populations diverged genetically from their ancestor and genetic diversity has accumulated within them (Papadopoulos et al., 1999). All of the populations achieved similar gains in competitive fitness, indicative of substantial adaptation, based on competition experiments with marked variants of the ancestor in the same glucose-limited environment (Lenski and Travisano, 1994; Cooper and Lenski, 2000). Several other phenotypic aspects also evolved in parallel including cell size (Lenski et al., 1998), growth parameters (Vasi et al., 1994), catabolic functions (Cooper and Lenski, 2000; Pelosi et al., 2006), DNA topology (Crozat et al., 2005), and global gene expression (Cooper et al., 2003).

In one of the populations, a cross-feeding polymorphism evolved where two morphs, called large (L) and small (S) based on their colony morphology, coexist in a frequency-dependent manner (Rozen and Lenski, 2000). Two factors enabled their coexistence, despite the fact that L grows exponentially about 20% faster than S. First, L excretes a metabolite that differentially promotes the growth of S. Second, L experiences increased death during stationary phase (i.e., after glucose is depleted) when S is present. The S and L morphs are both present from at least as early as generation 6.000 and they have continued to coexist for tens of thousands of generations. Interestingly, however, the relationship between the morphs is dynamic through time, with the frequency of S rising and falling several times from about 10-20% to about 50-90% of the total population. Restriction Fragment Length Polymorphism analyses, using Insertion Sequence elements to resolve the phylogenetic history of L and S, demonstrated that all of the S clones are monophyletic, indicating a long history of coexistence with L (Rozen et al., 2005). Moreover, competition assays using clones of both morphs from different generations, indicated that both lineages continued to adapt, and their continued evolution contributed to fluctuations in their relative abundance over evolutionary time. Based on their phylogenetic history and independent evolutionary trajectories, S and L fulfill one set of criteria for being different asexual species (Cohan, 2002).

This genome sequencing project aims to identify all of the mutations responsible for the divergence and maintenance of both asexual morphs, and therefore to understand mechanisms of microbial diversification and speciation. Moreover, the population from which these two morphs arose evolved a mutator phenotype, leading to an increase of about 100-fold in mutation rate (Sniegowski et al., 1997).

The genome of three different evolved clones will be sequenced at Genoscope: one clone isolated at 2.000 generations, hence before the emergence of the polymorphism, and one clone from each distinct morph isolated at 40.000 generations, to investigate the molecular mechanisms underlying their evolutionary divergence and coexistence. These genome sequences will be compared to the one of the ancestor clone, already available through a common sequencing effort between the Genoscope and the Korea Research Institute of Bioscience and Biotechnology (KRIBB, Dr. Jihyun F. Kim, Republic of Korea).

Contacts: Valérie Barbe (Genoscope) - Dominique Schneider (Université Joseph Fourier)

Bibliography

Cohan FM. 2002. What are bacterial species? Annu Rev Microbiol 56:457-487.

Cooper VS, Lenski RE. 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407:736-739.

Cooper TF, Rozen DE, Lenski RE. 2003. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci USA 100:1072-1077.

Crozat E, Philippe N, Lenski RE, Geiselmann J, Schneider D. 2005. Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169:523-532.

Lenski RE, Rose MR, Simpson SC, Tadler SC. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138:1315-1341.

Lenski RE, Travisano M. 1994. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci USA 91:6808-6814.

Lenski RE, Mongold JA, Sniegowski PD, Travisano M, Vasi F, et al. 1998. Evolution of competitive fitness in experimental populations of E. coli: What makes one genotype a better competitor than another? Antonie van Leeuwenhoek 73:35–47.

Lenski RE. 2004. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breed Rev 24:225-265.

Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M. 1999. Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci USA 96:3807-3812.

Pelosi L, Kühn L, Guetta D, Garin J, Geiselmann J, Lenski RE, Schneider D. 2006. Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173:1851-1869.

Philippe N, Crozat E, Lenski RE, Schneider D. 2007. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. BioEssays 29:846-860.

Rozen DE, Lenski RE. 2000. Long-Term Experimental Evolution in Escherichia coli. VIII. Dynamics of a Balanced Polymorphism. Am Nat 155:24-35.

Rozen DE, Schneider D, Lenski RE. 2005. Long-term experimental evolution in Escherichia coli. XIII. Phylogenetic history of a balanced polymorphism. J Mol Evol 61:171-180.

Sniegowski PD, Gerrish PJ, Lenski RE. 1997. Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387:703-705.

Vasi F, Travisano M, Lenski RE. 1994. Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am Nat 144:432-456.

Last update on 15 January 2008

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