Cohan FM, Perry EB.. A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17: R373-R386

Department of Biology, Wesleyan University, Middletown, Connecticut 06459-0170, USA.
Current Biology (Impact Factor: 9.57). 06/2007; 17(10):R373-86. DOI: 10.1016/j.cub.2007.03.032
Source: PubMed


Bacterial systematists face unique challenges when trying to identify ecologically meaningful units of biological diversity. Whereas plant and animal systematists are guided by a theory-based concept of species, microbiologists have yet to agree upon a set of ecological and evolutionary properties that will serve to define a bacterial species. Advances in molecular techniques have given us a glimpse of the tremendous diversity present within the microbial world, but significant work remains to be done in order to understand the ecological and evolutionary dynamics that can account for the origin, maintenance, and distribution of that diversity. We have developed a conceptual framework that uses ecological and evolutionary theory to identify the DNA sequence clusters most likely corresponding to the fundamental units of bacterial diversity. Taking into account diverse models of bacterial evolution, we argue that bacterial systematics should seek to identify ecologically distinct groups with evidence of a history of coexistence, as based on interpretation of sequence clusters. This would establish a theory-based species unit that holds the dynamic properties broadly attributed to species outside of microbiology.

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    • "Driven by positive selection, dnaE2 passes through one bacterium to another (by horizontal gene transfer or recombination), sweeping through different bacterial phyla and triggering new ecological differentiations. This view is consistent with the model of 'ecotype-formation mutations' (Cohan and Perry, 2007). However, significant work remains to be done in order to reveal the detailed genetic basis of these adaptive evolutionary changes. "
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    ABSTRACT: Exploring molecular mechanisms underlying bacterial water-to-land transition represents a critical start toward a better understanding of the functioning and stability of the terrestrial ecosystems. Here, we perform comprehensive analyses based on a large variety of bacteria by integrating taxonomic, phylogenetic and metagenomic data, in the quest for a unified view that elucidates genomic, evolutionary and ecological dynamics of the marine progenitors in adapting to nonaquatic environments. We hypothesize that bacterial land colonization is dominated by a single-gene sweep, that is, the emergence of dnaE2 derived from an early duplication event of the primordial dnaE, followed by a series of niche-specific genomic adaptations, including GC content increase, intensive horizontal gene transfer and constant genome expansion. In addition, early bacterial radiation may be stimulated by an explosion of land-borne hosts (for example, plants and animals) after initial land colonization events.The ISME Journal advance online publication, 23 January 2014; doi:10.1038/ismej.2013.247.
    Full-text · Article · Jan 2014 · The ISME Journal
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    • "Ecotype formation occurs when an individual changes its ecological niche, thereby releasing itself from the cohesive force of periodic selection within its parental ecotype. Ecotype formation is therefore analogous to sexual isolation and speciation among macroorganisms (8,42). Estimating the rates of periodic selection and ecotype formation therefore can shine light on the evolutionary and ecological processes that drive microbial diversity. "
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    ABSTRACT: The lack of a consensus bacterial species concept greatly hampers our ability to understand and organize bacterial diversity. Operational taxonomic units (OTUs), which are clustered on the basis of DNA sequence identity alone, are the most commonly used microbial diversity unit. Although it is understood that OTUs can be phylogenetically incoherent, the degree and the extent of the phylogenetic inconsistency have not been explicitly studied. Here, we tested the phylogenetic signal of OTUs in a broad range of bacterial genera from various phyla. Strikingly, we found that very few OTUs were monophyletic, and many showed evidence of multiple independent origins. Using previously established bacterial habitats as benchmarks, we showed that OTUs frequently spanned multiple ecological habitats. We demonstrated that ecological heterogeneity within OTUs is caused by their phylogenetic inconsistency, and not merely due to 'lumping' of taxa resulting from using relaxed identity cut-offs. We argue that ecotypes, as described by the Stable Ecotype Model, are phylogenetically and ecologically more consistent than OTUs and therefore could serve as an alternative unit for bacterial diversity studies. In addition, we introduce QuickES, a new wrapper program for the Ecotype Simulation algorithm, which is capable of demarcating ecotypes in data sets with tens of thousands of sequences.
    Full-text · Article · Apr 2013 · Nucleic Acids Research
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    • "Studying in situ diversity of a given group of microbes is indeed problematic and providing a comprehensive study of any type of biological diversity would be complicated beyond feasibility if nearly every individual organism were ecologically unique [30]. "
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    ABSTRACT: Among abundant freshwater Betaproteobacteria, only few groups are considered to be of central ecological importance. One of them is the well-studied genus Limnohabitans and mainly its R-BT subcluster, investigated previously mainly by fluorescence in situ hybridization methods. We designed, based on sequences from a large Limnohabitans culture collection, 18 RLBH (Reverse Line Blot Hybridization) probes specific for different groups within the genus Limnohabitans by targeting diagnostic sequences on their 16 S-23 S rRNA ITS regions. The developed probes covered in sum 92% of the available isolates. This set of probes was applied to environmental DNA originating from 161 different European standing freshwater habitats to reveal the microdiversity (intra-genus) patterns of the Limnohabitans genus along a pH gradient. Investigated habitats differed in various physicochemical parameters, and represented a very broad range of standing freshwater habitats. The Limnohabitans microdiversity, assessed as number of RLBH-defined groups detected, increased significantly along the gradient of rising pH of habitats. 14 out of 18 probes returned detection signals that allowed predictions on the distribution of distinct Limnohabitans groups. Most probe-defined Limnohabitans groups showed preferences for alkaline habitats, one for acidic, and some seemed to lack preferences. Complete niche-separation was indicated for some of the probe-targeted groups. Moreover, bimodal distributions observed for some groups of Limnohabitans, suggested further niche separation between genotypes within the same probe-defined group. Statistical analyses suggested that different environmental parameters such as pH, conductivity, oxygen and altitude influenced the distribution of distinct groups. The results of our study do not support the hypothesis that the wide ecological distribution of Limnohabitans bacteria in standing freshwater habitats results from generalist adaptations of these bacteria. Instead, our observations suggest that the genus Limnohabitans, as well as its R-BT subgroup, represent ecologically heterogeneous taxa, which underwent pronounced ecological diversification.
    Full-text · Article · Mar 2013 · PLoS ONE
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