PERSPECTIVES Life should instead be described as a Web OPINION of Life15. It has also been suggested that a microbial niche can be changed after a single The ecological coherence of high HGT event16. However, there is a growing body of literature showing that HGT takes bacterial taxonomic ranks place mostly between closely related spe- cies because of reduced genetic barriers17. In addition, there is evidence that many high Laurent Philippot, Siv G. E. Andersson, Tom J. Battin, James I. Prosser, taxonomic levels of bacteria show ‘ecological Joshua P. Schimel, William B. Whitman and Sara Hallin coherence’ (REFS 18,19). Ecological coherence of a taxon means that the members of that Abstract | The species is a fundamental unit of biological organization, but its taxon share general life strategies or traits relevance for Bacteria and Archaea is still hotly debated. Even more controversial that distinguish them from members of other is whether the deeper branches of the ribosomal RNA-derived phylogenetic tree, taxa. Some obvious examples of shared life such as the phyla, have ecological importance. Here, we discuss the ecological strategies among high taxonomic groups are coherence of high bacterial taxa in the light of genome analyses and present found in the phylum Cyanobacteria, in which all members are capable of photoautotrophic examples of niche differentiation between deeply diverging groups in terrestrial growth, and the phylum Chlamydiae, in and aquatic systems. The ecological relevance of high bacterial taxa has implications which all known members are obligate intra- for bacterial taxonomy, evolution and ecology. cellular symbionts or parasites of eukaryotes. If we assume that adaptations to different If you have ever read a field guide for birds, ribosomal RNA (rRNA) sequences to infer ecological niches have shaped and differen- mammals or plants, you will have noticed phylogenies, through which he proposed a tiated bacterial genetic lineages during the that it includes not only a description of each natural system that sorted organisms into course of evolution, then these divergences organism but also a wealth of information three domains of life: Bacteria, Archaea and should be reflected not only at the strain or about their habitat, geographical distribu- Eukarya8. Attempts to attribute ecologi- species level but also at higher taxonomic tion and ecological traits. Such information cal traits to bacterial and archaeal groups ranks. However, ecological coherence can is available at the species level as well as at that are defined at taxonomic ranks higher be confounded by selective pressures act- high taxonomic levels, such as the phylum. than species are rare, and the idea that the ing on different niches, resulting in different A field guide for bacteria might sound far- deep branches of the bacterial and archaeal genomes even for bacteria that share a com- fetched, considering that the number of trees could be ecologically coherent has mon evolutionary history. Moreover, selec- bacterial species that have been described is seldom been considered9. There are sev- tive constraints can also drive convergent low (~7,000)1 in relation to the millions of eral reasons for this. Genetic diversity is evolution, producing bacterial species that bacterial species that have been predicted much greater in the domains Bacteria and are functionally similar despite their differ- to reside on Earth2. However, the current Archaea than in the kingdom Metazoa. ent evolutionary histories. For these reasons, limitations for such a guide are not only For example, the percentage of conserved the question of whether ecological coherence the enormous diversity of bacteria but also genes between strains of the bacterial spe- exists at deeper evolutionary divergences our lack of knowledge about the ecology of cies Ralstonia solanacearum can be as low also addresses the fundamental evolutionary each of the known species. We do not know as 68%10, whereas 75% of human genes processes that have shaped such lineages. the distribution of most bacteria in nature, have homologues in the genome of the fish In this Opinion article, we examine and we do not know what they are actually Takifugu rubripes11. Likewise, there can be whether there is ecological coherence of bac- doing in their natural environments. In fact, substantial physiological diversity within terial taxonomic ranks higher than the species we cannot even define the niche of the best bacterial clades; for example, the phylum level. First, we discuss the ecological coher- studied bacterial species, Escherichia coli3,4. Proteobacteria includes heterotrophs, ence of various bacterial clades in the light of These difficulties are intertwined with our lithotrophs and phototrophs. In bacteria, genome analyses. Next, we highlight studies struggle to apply the species concept to ecological traits can be strain specific, and that support the ecological relevance of high bacteria1,5–7. closely related bacteria can occupy distinct bacterial taxa in terrestrial and aquatic sys- Ever since bacteria were discovered, the niches12,13. Furthermore, horizontal gene tems. Finally, we discuss the implications of question of whether they form phyloge- transfer (HGT) can occur even between these data for bacterial taxonomy, evolution netically coherent units and the extent to distantly related organisms14. In fact, some and ecology. We focus here on the domain which such units correlate with phenotypic authors claim that HGT is so rampant that Bacteria, but the same proposal of ecological characteristics and environmental adapta- no natural classification system can be coherence of high taxonomical ranks can also tions have been debated. Carl Woese used described for bacteria and that the Tree of be made for Archaea. NATURE REVIEWS | MICROBIOLOGY VOLUME 8 | JULY 2010 | 523 © 2010 Macmillan Publishers Limited. All rights reserved PERSPECTIVES A genomic perspective and gene content-based trees at high taxo- of photosynthetic genes is easy to associ- Currently, more than 1,000 bacterial nomic ranks23 suggests that a large fraction ate with the lifestyle of the Cyanobacteria. genomes have been completely sequenced, of bacterial genomes reflect an underlying However, genomic signatures of more com- and there are several hundred ongoing pattern of vertical gene descent. plex phenotypes such as virulence, thermo- bacterial genome projects at various stages One approach of examining the depth phily or radiation resistance have been more of completion (see Further information for of ecological coherence and the genomic difficult to delineate28. Moreover, many links). Although the collection of species changes associated with lifestyle shifts is to signature genes encode proteins of unknown for which genomes are available is biased superimpose recently acquired functional function, which might not necessarily be towards bacteria that are important to traits and ecological adaptations onto a tree involved in environmental adaptation. human health and agriculture, pilot projects that displays vertical descent. The simplest How much ecological diversity is there that advocate the sequencing of genomes expectation is that all members of ecologi- within a taxonomically defined bacterial lin- solely for their phylogenetic novelty, such cally coherent clades will share a unique set eage? The class Alphaproteobacteria, which as the Genomic Encyclopaedia of Bacteria of genes24 and, indeed, such genes have been has more than 100 sequenced representa- and Archaea (GEBA) project, are in identified for some taxonomic clades. For tives, is one of the most ecologically diverse progress and promise to generate a more example, around 120 of the 1,054 core genes classes and is therefore a particularly good balanced and useful data set20. This makes it identified for the Cyanobacteria are spe- model system to use to address this ques- timely to pose questions about the levels in cific to this phylum25. Likewise, 233 and 51 tion29. An alphaproteobacterial species tree the taxonomic hierarchy that display coher- signature genes have been reported for the has been inferred from concatenated data ence in lifestyle and about whether such phyla Actinobacteria and Chlorobi, respec- sets of 38 and 102 protein-coding genes30,31. clades share unique ecological traits. tively26,27. For the phylum Bacteroidetes, On the basis of this tree, a divergence pat- Genome sequence data enable the con- the order Bacteroidales and the genus tern has been inferred for the major bacte- struction of sequence-based phylogenies Bacteroides, 27, 38 and 185 signature genes, rial orders within the Alphaproteobacteria, for all genes in the genome and have led to respectively, have been identified27. The including the Rickettsiales, Rhodospirillales, the emergence of a new field of research: number of signature genes tends to be Sphingomonadales, Caulobacterales, phylogenomics21,22. Work in this field offers negatively correlated with taxonomic rank, Rhodobacterales and Rhizobiales. The insights into the mechanisms by which as exemplified above, with fewer signature habitats of a few species from each of these bacterial genomes change and adapt to new genes at the order level than at the genus orders are shown in FIG. 1. Although many environments. Core genes encoding proteins level and even fewer at the phylum level. It lifestyles and environments are represented, involved in basic information processes is also likely that the number of signature distinct patterns