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REVIEWS

Microbial diversity and the genetic nature of microbial species
Mark Achtman* and Michael Wagner‡

Abstract | The earth contains a huge number of largely uncharacterized Bacteria and Archaea. Microbiologists are struggling to summarize their genetic diversity and classify them, which has resulted in heated debates on methods for defining species, mechanisms that lead to speciationand whether microbial species even exist. This Review proposes that decisions on the existence of species and methods to define them should be guided by a method-free species concept that is based on cohesive evolutionary forces. It summarizes current approaches to defining species and the problems of these approaches, and presents selected examples of the population genetic patterns at and belowthe species level.
Homologous recombination
The acquisition of DNA segments from closely related microbes via recombination at flanking homologous sequence stretches.

Lateral gene transfer
The acquisition of novel DNA segments from unrelated sources.

Operational taxonomic unit
Usually defined as the number of distinct 16S ribosomal RNA sequences at a certain cut-off level of sequencediversity.

*Environmental Research Institute, University College Cork, Ireland and Department of Molecular Biology, Max‑Planck Institut für Infektionsbiologie, 10117 Berlin, Germany. ‡ Department of Microbial Ecology, Faculty of Life Sciences, Vienna Ecology Centre, University of Vienna, A‑1090 Vienna, Austria. Correspondence to M.A. e‑mail: m.achtman@ucc.ie doi:10.1038/nrmicro1872 Published online7 May 2008

The classification system developed by Carl Linnaeus extended to animals, plants and rocks. Linnaeus did not classify microbes, used in this Review to refer col‑ lectively and exclusively to Bacteria and Archaea1, but since the mid‑nineteenth century, binomial Linnaean names have been used by microbiologists to designate microbial species. The species level is where multipledisciplines intersect, including microbial systematics, ecology, population genetics, evolution and genomics. The explosion of data during the genomic era has been accompanied by debates that threaten the existence of any cohesive overview of the genetic nature of microbial species. Furthermore, the newly appreciated importance of the frequency of recombination, either in the form of homologousrecombination2 or lateral gene transfer (LGT)3, has challenged our concepts in each field and has raised many questions. It is difficult to integrate these diverse sources of information, because microbiologists lack a widely accepted theoretical species concept that is com‑ parable to the biological species concept proposed by Ernst Mayr4. According to the biological species concept, the existence of manyanimal species and some plant spe‑ cies is ensured by the cohesive evolutionary forces that result from pre‑zygotic and post‑zygotic barriers between eukaryotic species5. Cohesive evolutionary forces are also necessary to generate microbial species, because in their absence the accumulation of genetic variation would probably result in a genetic continuum and microbial species would represent anartificial classification rather than a natural, circumscribed biological grouping3. Microbial species are currently defined by a prag‑ matic, polyphasic approach that is based on clear rules for both genotypic and phenotypic properties6 (BOX 1).

This pragmatic approach has served the community well, resulting in more than 7,031 accepted microbial species (G.M. Garrity, personal communication),and is being adapted to the genomic era. However, as currently practised, this approach faces serious problems, because a primary criterion for distinguishing species is a certain cut‑off level for pairwise genomic DNA–DNA hybridi‑ zation levels. This cut‑off level is not based on any par‑ ticular theoretical justification, but instead was chosen 20 years ago to match pre‑existing species...
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