Wednesday, October 3, 2012

Evolutionary consequences of sex: It's not about what you're doing, but who you're doing it with...
Bacteria are one of the most ubiquitous living group and exhibit finely tuned adaptations to a wide range of habitats, even the most inhospitable ones. Their ability to evolve rapidly is at the roots of many public health issues, such as the development of resistances to antibiotics or the rapid evolution of seasonal diseases, but can also be of great help to humans by creating new metabolic pathways to transform human-made pollutants and harmful substances. In the early 20th century, new bacterial genomes were still thought to be the result of mutations only, and to be then transmitted vertically within a clonal strain. In the 40’s, the discovery of bacterial DNA recombination through transformation (Avery, MacLeod and McCarty experiment in 1944) or conjugation (Lederberg and Tatum experiment in 1946) shed light on the processes responsible for the rapid ecological differentiation of bacterial strains: an individual can acquire new genes or alleles through recombination that allow it to stand new ecological conditions.

In Eucaryotes, genetic exchange and recombination through sexual reproduction is considered the basis of gene-specific transmission and selection among a population. However, the importance of genetic exchange between bacteria in uncoupling selection processes between different genes remains a controversial issue. In fact, contradictory observations have elicited two models of selection:
  1. On one hand, the ecological clustering of bacterial biodiversity in genetically consistent ecotypes support the traditional view that adaptive mutations are selected through whole-genome clonal selection. Moreover the low measured levels of recombination are insufficient to unlink a gene from the rest of the genome.
  2. On the other hand, the existence of environment specific genes and alleles suggests that recombination can unlink parts of the genome. Moreover, some loci exhibit low nucleotidic diversities compared to the rest of the genome, with suggest purifying selection on these regions. Thus adaptive mutations seems to be selected quite independently of the rest of the genome.
To disentangle those apparently incompatible observations and assess the degree of gene uncoupling in bacteria, researchers of the MIT examined in a recently published study[i] the genomes of 20 strains representing two ecotypes in the marine species Vibrio cyclitrophicus. As the genomes of these ecotypes are extremely similar, they can be considered the result of recent ecological differentiation, thus giving us a snapshot of this evolutionary process. Based on the comparison of these sequences, the authors claim that gene-specific sweeps do occur and can lead to environment specific-genes on a short time scale, but also to ecological clustering, through preferential within-habitat recombination, on a longer time scale.

In fact, different parts of the genome have different evolutionary histories. Especially, ecotype-specific SNPs are only found on a few locations in the genome, whereas the rest of the polymorphic genome supports a genetic intermingling between the ecotypes. Moreover, the two chromosomes of V. cyclitrophicus support different phylogenies, with chromosome 1 grouping the ecotypes, whereas chromosome 2 splits one ecotype into two groups. The phylogeny within one of these two groups is strongly supported by chr2 but not by chr1. Thus, habitat-specific genes are evolving quite independently and do not drive genomewide selective sweeps, an observation consistent with the environment specific genes and alleles that have already been documented[ii].

These results highlight the need for high quality sequencing data and fine grained analysis to understand the evolutionary histories of different parts of the genome. In fact, the authors show that a few loci with consistent phylogeny, such as the ecotype-specific SNPs here, are sufficient to drive the whole-genome phylogeny, if the signal of clonal ancestry in the rest of the genome has been blurred by homologous recombination (Fig. 1). Therefore, the ecotype theory might be based on phylogenies biased toward the history of a few loci under purifying habitat-driven selection rather than on neutral loci with inconsistent histories accounting for most of the genome.

Fig. 1: A. Maximum-likelihood phylogeny for the core genome (genes presents in all strains) of chromosome I in V. cyclitrophicus. Scale is substitution per site. All nodes have a 100% bootstrap support unless indicated. B. Genome regions with uninterrupted support for (black points) or against (grey points) the ecological split. ML trees for three major regions are shown. Adapted from Shapiro et al. 2012.

The most important point made by the authors remains however their evidences for preferential within-ecotype recombination. When examining recombination events affecting recently diverged pairs of strains, recombination rates were found to be higher within than between habitats. The authors make here an essential point toward a unified theory of bacterial genomes evolution. Such preferential recombination indeed provides an explanation for the development of ecotypes, usually considered an evidence of genomewide genetic sweeps, from gene-specific sweeps. Even if the mechanisms involved in genes transmission are quite different between Eubacteria and Eucaryotes, they seem to converge in allowing gene-specific selective sweeps and in restricting genetic exchange between habitat. This study show a more universal picture of selective pressures on evolutionary mechanisms than previously thought between Eucaryotes and Eubacteria (Fig. 2).

Fig. 2: Model of ecological differentiation between bacterial ecotypes (from Shapiro et al. 2012). Thin grey (resp. black) arrows represent recombination within (resp. between) ecologically associated populations. Thick coloured arrows represent acquisition of adaptive alleles for red or green habitat.

Eventually, this new insight into bacterial evolution plead for a new structure of bacterial diversity. Whether and how a species-level could be defined in Eubacteria has been a long standing controversy. The current species criterion dates back to 1987: it defines a species as a group of clonal strains characterized by at least one phenotypic trait and 70% DNA–DNA hybridization[iii]. However this definition was often criticized for grouping within one species extremely diverse phenotypes[iv]. Moreover, the very idea of bacterial species was sometimes rejected on the basis of common genetic exchanges between morphologically and ecologically distinct bacteria[v]. That last assertion is here contradicted by demonstrating the existence of barriers to gene flow between habitats. If recombination, that is “bacterial sex”, is more frequent within than between habitats, ecotypes are quite close to the definition of a species in Eucaryotes, an “ecotype-hypothesis” already put forward about ten years ago[vi]. Therefore this study provides a first step toward the “solid understanding of the genetic basis of the ecological distinctiveness of the ecotype” advocated by Konstantinidis et al. in 2006[iv], although it does not exclude the possibility that some ecotypes be defined by gene expression rather than gene content.

New paths for research are here opened, especially to define the barriers to gene flow that could explain habitat-specific recombination. The bacteria studied here are not known well enough to define the ecological differentiation observed as sympatric or allopatric: if their habitats within sea water are distinct enough, a physical barrier could be considered. If the differentiation can be regarded as sympatric, the mechanisms that prevent recombination between ecotypes are still to be investigated.

[i] Shapiro B.J. et al. (2012). Population genomics of early events in the ecological differentiation of bacteria. Science 336:48-51.
[ii] Coleman M.L. and Chisholm S.W. (2010). Ecosystem-specific selection pressures revealed through comparative population genomics. Proc. Natl. Acad. Sci. U.S.A. 107(43):18634-18639.
[iii] Wayne L.G. et al. (1987). Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int. J. Syst. Bacteriol. 37:463-464.
[iv] Konstantinidis K.T., Ramette A. and Tiedje J.M. (2006). The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci. 361(1475): 1929-1940.
[v] Margulis L. and Sagan D. (1997). Microcosmos: Four Billion Years of Microbial Evolution. University of California Press.
[vi] Cohan F.M. (2002). What are bacterial species? Annu Rev Microbiol. 56:457-487.
Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, Polz MF, & Alm EJ (2012). Population genomics of early events in the ecological differentiation of bacteria. Science (New York, N.Y.), 336 (6077), 48-51 PMID: 22491847

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