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:
- 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.
- 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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