Opinion Lateral gene transfer challenges principles of microbial systematics Eric Bapteste1 and Yan Boucher2 1 UPMC UMR 7138, 7 quai Saint-Bernard, Baˆ timent A, 4e`me e´ tage, 75005, Paris, France 2 Department of Civil and Environmental Engineering, MIT, Building 48–305, 77 Massachusetts Avenue, Cambridge, MA 02139, USA Evolutionists strive to learn about the natural historical As a result, the traditional TOL reconstruction project, process that gave rise to various taxa, while also as far as prokaryotic organisms are concerned, fell short. It attempting to classify them efficiently and make gener- is arguable whether debating the branching order in the alizations about them. The quantitative importance of TOL and looking for a unique nested hierarchy is a satis- lateral gene transfer inferred from genomic data, factory way to classify such microbes in the presence of although well acknowledged by microbiologists, is in lateral gene transfer. Instead, we propose alternative con- conflict with the conceptual foundations of the cepts to the traditional phylogenetic projects to deal with traditional phylogenetic system erected to achieve these microbial evolution and systematics: (i) a redefinition of goals. To provide a true account of microbial evolution, natural groups; (ii) the description of a new type of evol- we suggest developing an alternative conception of utionary unit originating from lateral gene transfer (LGT); natural groups and introduce a new notion – the com- and (iii) the realization of an interactive taxonomical data- posite evolutionary unit. Furthermore, we argue that a base (comprising overlapping groups) to progress towards comprehensive database containing overlapping taxo- a more natural classification. The third of these solutions nomical groups would constitute a step forward regard- would constitute a transition possibly as significant as the ing the classification of microbes in the presence of change from a linear system of classification to a nested lateral gene transfer. hierarchy that occurred thousands of years ago. Introduction The molecular phylogenetics project conceived by Zucker- Glossary kandl and Pauling [1] in the 1960s was ambitious. Among Essentialism: the view that some permanent, unalterable properties other revolutionary accomplishments, molecular phyloge- of objects are essential to them, so that, for any specific type of entity, netics was expected to function as a powerful time machine, it is at least theoretically possible to specify a finite list of character- enabling the identification of genetic, ultrastructural and istics – all of which must be possessed by any entity to belong to the metabolic features of ancient life forms for which no fossils group defined. For instance, for a property essentialist, all essential parts of a species remain unchanging throughout time. In historical had been left [2]. Through their congruence (i.e. the agree- essentialism, the unchanging essential characteristic is a common ment between phylogenies obtained using different data- history. A monophyletic group is thus natural because it is defined by sets) [2], genes could help to reconstruct what is often called the existence of a last common ancestor exclusively shared by all its the Tree of Life (TOL). To understand ancient microbial members, even though these members are not similar to each other in other respects (ecologically, morphologically, functionally etc.). evolution, the biggest challenges have been seen as mostly Mill, John Stuart: British philosopher (1806–1873) who was an influ- methodological – improving phylogenetic algorithms accu- ential liberal thinker. He is notably famous for his defense of utilitar- rately to model the complex evolution of molecules [3] and ianism and his book A System of Logic: Ratiocinative and Inductive, sequencing a sufficient number of phylogenetic markers [4]. published in 1843, describing the five basic principles of induction Using a wealth of methods and data, TOLs flourished [5,6]. and the methods of scientific inquiry. Monism: at the methodological level, the view that a single method Yet, over the past 15 years, lateral inheritance (as opposed to and a unique representation can account satisfactorily for the unified vertical descent) was discovered to be a major evolutionary set of laws that underlie nature. force in microorganisms [7–11]. For archaea, bacteria and Pluralism: opposes monism by endorsing the view that several some unicellular eukaryotes, individual gene histories can methods and theories are legitimate in an evolutionary study legitimately differ from species history, and the two phylo- because no single coherent explanatory system can account satis- factorily for all the diverse phenomena of life. genetic patterns (species trees and gene trees) do not have to Polythetic: a phylogenetic group in which ‘(i) each individual has a show much identity with one another on a broad evolution- large but unspecified number of a set of properties occurring in the ary scale. Microbial physiologists and geneticists were not aggregate as a whole; (ii) each of those properties is possessed by surprised by the fact that a single genome could comprise large numbers of those individuals; (iii) not one of those properties is genes arising from multiple phylogenetic sources, yet it possessed by every individual in the aggregate’, as explained in Ref. [46]. conflicted with the conceptual foundations of the phyloge- Synapomorphy: a derived character state shared by two or more netic system. terminal groups (taxa included in a cladistic analysis as further indivisible units) and inherited from their most recent common ancestor. Corresponding author: Bapteste, E. ([email protected]). 200 0966-842X/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tim.2008.02.005 Available online 15 April 2008 Opinion Trends in Microbiology Vol.16 No.5 Box 1. Different types of evolutionary trees Box 2. LGT and the definition of natural groups Two types of evolutionary trees are currently being reconstructed. Consider four organisms, in two independently evolving lineages: First are genome trees, based on the statistical properties of the two photobacteria (P1 and P2) having photoreceptors; and two genome, on the presence or absence of genes, on the chromosomal flagellobacteria (F3 and F4) harboring a flagellum (see Figure 1 in gene order or on average sequence similarity, as calculated in the main text). Suppose that, at t1, a descendant from P2 laterally BLAST analyses (and variants thereof). Second are phylogenomic acquired a flagellum it obtained from an F4 relative in addition to its trees, based on vertically inherited orthologs [17]. Genome trees photoreceptors. How should the chimeric P2 descendant be provide a way to compare the evolutionary information present in classified? Multiple answers seem possible: (i) because it harbors different genomes. However, they do not reflect the exact course of photoreceptors, the P2 descendant could be joined to the photo- organismal evolution and should not be interpreted as phylogenies. bacteria; (ii) because it harbors a flagellum, the P2 descendant could In no case is the relevance of the tree model tested in these be joined to the flagellobacteria; (iii) because it presents both approaches. Furthermore, such phenetic trees are especially com- photoreceptors and a flagellum, the P2 descendant is something plex to interpret because some of the groupings obtained can result new, neither a photobacteria nor a flagellobacteria. Evolutionists principally from lateral relationships, whereas others result from generally rely on historical evidence, and consider the photorecep- vertical ones. In summary, genome trees show prevailing trends in tors as a synapomorphy, the flagellum as a bad character for natural the evolution of genome-scale gene sets [16].Bycontrast, classification, and the P2 descendant as ‘a photobacterium that phylogenomic Trees – species Trees – are reconstructed to learn acquired a flagellum’ (the exact description of its evolutionary about the pattern of natural relationships between species [18,19] history). on the basis of strictly vertically inherited markers. To this end, Suppose now that, later, at t2, the P2 descendant lost its molecular datasets are trimmed to exclude genes with conflicting photoreceptors. Then, the P2 descendant would only harbor a signals. There are, however, very few data for which one can flagellum, homologous to those found in F4 and F3 descendants. confidently assess a strictly vertical transmission, resulting in Would it be considered a flagellobacteria? This would seem the skeletal microbial phylogenomic trees, built on a very small amount most natural solution, given the presence of a flagellum, which is of information. The latest TOL, published by Ciccarelli et al. [6], the essence of the flagellobacteria category, and the absence of which Dagan and Martin legitimately renamed the ‘tree of one per other traits that would suggest an alternative classification. Yet, it cent’ [20], is a good example of this. In addition, this approach is would be in direct contradiction with the historical logic used at t1, probably unwillingly essentialist, because a few characters are according to which ‘being a photobacterium’ means to have a last being reified in the name of the congruence between the gene trees common ancestor that had photoreceptors, regardless of the make- and the species tree. Such a definition makes genes the essence of up of the extant