The bacterial species challenge: making sense of genetic and ecological diversity.
ABSTRACT The Bacteria and Archaea are the most genetically diverse superkingdoms of life, and techniques for exploring that diversity are only just becoming widespread. Taxonomists classify these organisms into species in much the same way as they classify eukaryotes, but differences in their biology-including horizontal gene transfer between distantly related taxa and variable rates of homologous recombination-mean that we still do not understand what a bacterial species is. This is not merely a semantic question; evolutionary theory should be able to explain why species exist at all levels of the tree of life, and we need to be able to define species for practical applications in industry, agriculture, and medicine. Recent studies have emphasized the need to combine genetic diversity and distinct ecology in an attempt to define species in a coherent and convincing fashion. The resulting data may help to discriminate among the many theories of prokaryotic species that have been produced to date.
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ABSTRACT: Bacterial genomes are mosaics with fragments showing distinct phylogenetic origins or even being unrelated to any other genetic information (ORFan genes). Thus the analysis of bacterial population genetics is in large part a collection of explanations for anomalies in relation to classical population genetic models such as the Wright-Fisher model and the Kingman coalescent that do not adequately describe bacterial population genetics, genomics or evolution. The concept of "species" as an evolutionary coherent biological group that is genetically isolated and shares genetic information through recombination among its members cannot be applied to any bacterial group. Recently, a simple probabilistic model considering the role of strong seed-bank effects in population genetics has been proposed by Blath et al. This model suggests the existence of a genetic pool with high diversity that is not subject to classical selection and extinction. We reason that certain bacterial population genetics anomalies could be explained by the prevalence of strong seed-bank effects among bacteria. To address this possibility we analyzed the genome of the bacterium Azotobacter vinelandii and show that genes that code for functions that are essential for the bacterium biology do not have a relation of ancestry with closely related bacteria, or are ORFan genes. The existence of essential genes that are not inherited from the most recent ancestor cannot be explained by classical population genetics models and is irreconcilable with the current view of genes acquired by horizontal transfer as being accessory or adaptive.Journal of Theoretical Biology 04/2014; · 2.35 Impact Factor
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ABSTRACT: Recent advances such as high-throughput sequencing (HTS) have changed conceptions about the magnitude of diversity on Earth. This is especially true for microbial lineages, which have seen the discovery of great numbers of rare forms in places such as the human gut as well as diverse environments (e.g., freshwater, marine, and soil). Given the differences in perceptions of diversity for bacterial and eukaryotic microbes, including divergent species concepts, HTS tools used to eliminate errors and population-level variation in bacteria may not be appropriate for microbial eukaryotes and may eliminate valid species from the data. We discuss here how the nature of biodiversity varies among microbial groups and the extent to which HTS tools designed for bacteria are useful for eukaryotes.Trends in Microbiology 05/2014; · 8.43 Impact Factor
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ABSTRACT: Many antagonistic interactions between hosts and their parasites result in coevolution. Although coevolution can drive diversity and specificity within species, it is not known whether coevolutionary dynamics differ among functionally similar species. We present evidence of coevolution within simple communities of Pseudomonas aeruginosa PAO1 and a panel of bacteriophages. Pathogen iden-tity affected coevolutionary dynamics. For five of six phages tested, time-shift assays revealed temporal peaks in bacterial resistance and phage infectivity, consistent with frequency-dependent selection (Red Queen dynamics). Two of the six phages also imposed addi-tional directional selection, resulting in strongly increased resistance ranges over the entire length of the experiment (ca. 60 generations). Cross-resistance to these two phages was very high, independent of the coevolutionary history of the bacteria. We suggest that coevo-lutionary dynamics are associated with the nature of the receptor used by the phage for infection. Our results shed light on the coevolutionary process in simple communities and have practical application in the control of bacterial pathogens through the evo-lutionary training of phages, increasing their virulence and effi-cacy as therapeutics or disinfectants. phage therapy | nosocomial pathogen | fluctuating selection | arms race | type IV pili M any host–parasite associations coevolve, and patterns in this antagonistic interaction are influenced by biology and environment (1–3). In single-species host–parasite interactions, parasite genotypes show differences in their host ranges and specificities on host genotypes, providing the basis for such co-evolution (4–8). Arms race dynamics (ARD) driven by direc-tional selection favors a broader resistance range in the host against a greater number of parasite genotypes and an increased host range in the parasite allowing more host genotypes to be infected (2, 9). In contrast, fluctuating selection dynamics (FSD), in which there is no directional change in the evolution of the host resistance range, is governed by negative frequency-dependent selection, favoring hosts that resist the most frequently encountered parasite genotypes and parasites that infect the most common host genotypes (9–11). It has been suggested that ARD predominates during the initial stages of coevolution, when adaptations to the coevolving opponent are largely cost-free, whereas FDS is more significant at later stages, when attack/ defense alleles accumulate in the genome and impose costs (12). Thus, when systems shift from ARD to FSD, dynamic coevolu-tionary equilibria may arise, with constant numbers of attack/defense alleles at the individual level (13) and the continuous frequency-dependent (re)cycling of alleles at the population level (14). Coevolutionary dynamics between hosts and parasites is in-creasingly investigated using experimental evolution (15) and more specifically time-shift assays (16–18), in which hosts or parasites from a given time point are compared with their counterparts from the past or future, enabling the examination of putative reciprocal adaptations (19, 20). Some of the prime experimental models are bacteria and their lytic phages, which exhibit rapid evolution and are amenable to time-shift tests. Recent study indicates that coevolving populations may exhibit either ARD or FSD (12, 21–24), and there is some evidence for the genetic mechanism involved [e.g., mutations at tail fiber genes (12, 25)] and for the expansion of the phage host range as coevo-lution proceeds (6). Most studies of bacteria–phage coevolution involve the model system Pseudomonas fluorescens SBW25 and its lytic phage ϕ2 (15). Although these studies are important for an in-depth understanding of this process, their restriction to a single host–parasite pair is unfortunate, given the immense diversity of bacteria and phages in both terrestrial and aquatic ecosystems (26–28) and the importance of many of these organisms in human health (29). Thus, the generality of previous results to other bac-terial species and to different phages parasitizing a given bacte-rium remains an open question. Coevolution may be particularly important in an applied context, namely when predators or parasitic organisms are used for biocontrol (30). For instance, Conrad et al. (31) recently argued that a community perspective with its ecological and evolutionary underpinnings is needed to explore the usefulness of phages as antimicrobial agents to treat cystic fibrosis patients infected with several bacteria and notably strains of Pseudomonas aeruginosa, a congeneric to the model organism P. fluorescens. Different phages naturally have different host ranges (8, 32, 33), but whether phage taxonomic origin influences impacts on P. aeruginosa is not known. Despite the study of phage mixtures to control P. aeruginosa infections (34), the nature of bacterial cross-resistance to phages other than that with which the bac-terium evolved has not been addressed. Previous studies are inconclusive regarding whether P. aeruginosa coevolves with bacteriophages (35, 36). Given the ubiquity of thisProceedings of the National Academy of Sciences 07/2014; · 9.81 Impact Factor