Michiel Vos

A comparison of homologous recombination rates in bacteria and archaea.

It is a standard practice to test for the signature of homologous recombination in studies examining the genetic diversity of bacterial populations. Although it has emerged that homologous recombination rates can vary widely between species, comparing the results from different studies is made difficult by the diversity of estimation methods used. Here, Multi Locus Sequence Typing (MLST) datasets from a wide variety of bacteria and archaea are analyzed using the ClonalFrame method. This enables a direct comparison between species and allows for a first exploration of the question whether phylogeny or ecology is the primary determinant of homologous recombination rate.

Micro-scale determinants of bacterial diversity in soil

Soil habitats contain vast numbers of microorganisms and harbor a large portion of the planets biological diversity. Although high-throughput sequencing technologies continue to advance our appreciation of this remarkable phylogenetic and functional diversity, we still have only a rudimentary understanding of the forces that allow diverse microbial populations to coexist in soils. This conspicuous knowledge gap may be partially due the human perspective from which we tend to examine soilborne microorganisms. This review focusses on the highly heterogeneous soil matrix from the vantage point of individual bacteria. Methods describing micro-scale soil habitats and their inhabitants based on sieving, dissecting, and visualizing individual soil aggregates are discussed, as are microcosm-based experiments allowing the manipulation of key soil parameters. We identify how the spatial heterogeneity of soil could influence a number of ecological interactions promoting the evolution and maintenance of bacterial diversity.

Sociobiology of the Myxobacteria

Cooperation is integral to much of biological life but can be threatened by selfish evolutionary strategies. Diverse cooperative traits have evolved among microbes, but particularly sophisticated forms of sociality have arisen in the myxobacteria, including group motility and multicellular fruiting body development. Myxobacterial cooperation has succeeded against socially destructive cheaters and can readily re-evolve from some socially defective genotypes. However, social harmony does not extend far. Spatially structured natural populations of the model species Myxococcus xanthus have fragmented into a large number of socially incompatible genotypes that exclude, exploit, and/or antagonize one another, including genetically similar neighbors. Here, we briefly review basic social evolution concepts as they pertain to microbes, discuss potential benefits of myxobacterial social traits, highlight recent empirical studies of social evolution in M. xanthus, and consider their implications for how myxobacterial cooperation and conflict evolve in the wild.

Local adaptation of bacteriophages to their bacterial hosts in soil.

A host-parasite system indicates how ecological and evolutionary mechanisms shape the distribution of microbes in soil. Microbes are incredibly abundant and diverse and are key to ecosystem functioning, yet relatively little is known about the ecological and evolutionary mechanisms that shape their distributions. Bacteriophages, viral parasites that lyse their bacterial hosts, exert intense and spatially varying selection pressures on bacteria and vice versa. We measured local adaptation of bacteria and their associated phages in a centimeter-scale soil population. We first demonstrate that a large proportion of bacteria is sensitive to locally occurring phages. We then show that sympatric phages (isolated from the same 2-gram soil samples as the bacteria) are more infective than are phages from samples some distance away. This study demonstrates the importance of biotic interactions for the small-scale spatial structuring of microbial genetic diversity in soil.

Why do bacteria engage in homologous recombination

Microbiologists have long recognized that the uptake and incorporation of homologous DNA from outside the cell is a common feature of bacteria, with important implications for their evolution. However, the exact reasons why bacteria engage in homologous recombination remain elusive. This Opinion article aims to reinvigorate the debate by examining the costs and benefits that homologous recombination could engender in natural populations of bacteria. It specifically focuses on the hypothesis that homologous recombination is selectively maintained because the genetic variation it generates improves the response of bacterial populations to natural selection, analogous to sex in eukaryotes.

Discovering the Hidden Secondary Metabolome of Myxococcus xanthus: a Study of Intraspecific Diversity

ABSTRACT As a monophyletic group, the myxobacteria are known to produce a broad spectrum of secondary metabolites. However, the degree of metabolic diversity that can be found within a single species remains unexplored. The model species Myxococcus xanthus produces several metabolites also present in other myxobacterial species, but only one compound unique to M. xanthus has been found to date. Here, we compare the metabolite profiles of 98 M. xanthus strains that originate from 78 locations worldwide and include 20 centimeter-scale isolates from one location. This screen reveals a strikingly high level of intraspecific diversity in the M. xanthus secondary metabolome. The identification of 37 nonubiquitous candidate compounds greatly exceeds the small number of secondary metabolites previously known to derive from this species. These results suggest that M. xanthus may be a promising source of future natural products and that thorough intraspecific screens of other species could reveal many new compounds of interest.

Social Conflict in Centimeter-and Global-Scale Populations of the Bacterium Myxococcus xanthus

Social interactions among microbes that engage in cooperative behaviors are well studied in laboratory contexts [1, 2], but little is known about the scales at which initially cooperative microbes diversify into socially conflicting genotypes in nature. The predatory soil bacterium Myxococcus xanthus responds to starvation by cooperatively forming multicellular fruiting bodies in which a portion of the population differentiates into stress-resistant spores [3, 4]. Natural M. xanthus populations are spatially structured [5], and genetically divergent isolates from distant origins exhibit striking developmental antagonisms that decrease spore production in chimeric fruiting bodies [6]. Here we show that genetically similar isolates of M. xanthus from a centimeter-scale population [7] also exhibit strong and pervasive antagonisms when mixed in development. Negative responses to chimerism were less intense on average among local strains than among global isolates, although no significant correlation was found between genetic distance at multilocus sequence typing (MLST) loci and the degree of social asymmetry between competitors. A test for self/nonself discrimination during vegetative swarming revealed a great diversity of distinct self-recognition types even among identical MLST genotypes. Such nonself exclusion may serve to direct the benefits of cooperation to close kin within diverse populations in which the probability of social conflict among neighbors is high.

A comparison of rpoB and 16S rRNA as Markers in Pyrosequencing Studies of Bacterial Diversity.

Background The 16S rRNA gene is the gold standard in molecular surveys of bacterial and archaeal diversity, but it has the disadvantages that it is often multiple-copy, has little resolution below the species level and cannot be readily interpreted in an evolutionary framework. We compared the 16S rRNA marker with the single-copy, protein-coding rpoB marker by amplifying and sequencing both from a single soil sample. Because the higher genetic resolution of the rpoB gene prohibits its use as a universal marker, we employed consensus-degenerate primers targeting the Proteobacteria. Methodology/Principal Findings Pyrosequencing can be problematic because of the poor resolution of homopolymer runs. As these erroneous runs disrupt the reading frame of protein-coding sequences, removal of sequences containing nonsense mutations was found to be a valuable filter in addition to flowgram-based denoising. Although both markers gave similar estimates of total diversity, the rpoB marker revealed more species, requiring an order of magnitude fewer reads to obtain 90% of the true diversity. The application of population genetic methods was demonstrated on a particularly abundant sequence cluster. Conclusions/Significance The rpoB marker can be a complement to the 16S rRNA marker for high throughput microbial diversity studies focusing on specific taxonomic groups. Additional error filtering is possible and tests for recombination or selection can be employed.

Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale.

ABSTRACT Myxococcus xanthus is a gram-negative soil bacterium best known for its remarkable life history of social swarming, social predation, and multicellular fruiting body formation. Very little is known about genetic diversity within this species or how social strategies might vary among neighboring strains at small spatial scales. To investigate the small-scale population structure of M. xanthus, 78 clones were isolated from a patch of soil (16 by 16 cm) in Tübingen, Germany. Among these isolates, 21 genotypes could be distinguished from a concatemer of three gene fragments: csgA (developmental C signal), fibA (extracellular matrix-associated zinc metalloprotease), and pilA (the pilin subunit of type IV pili). Accumulation curves showed that most of the diversity present at this scale was sampled. The pilA gene contains both conserved and highly variable regions, and two frequency-distribution tests provide evidence for balancing selection on this gene. The functional domains in the csgA gene were found to be conserved. Three instances of lateral gene transfer could be inferred from a comparison of individual gene phylogenies, but no evidence was found for linkage equilibrium, supporting the view that M. xanthus evolution is largely clonal. This study shows that M. xanthus is surrounded by a variety of distinct conspecifics in its natural soil habitat at a spatial scale at which encounters among genotypes are likely.

Rates of Lateral Gene Transfer in Prokaryotes: High but Why?

Lateral gene transfer is of fundamental importance to the evolution of prokaryote genomes and has important practical consequences, as evidenced by the rapid dissemination of antibiotic resistance and virulence determinants. Relatively little effort has so far been devoted to explicitly quantifying the rate at which accessory genes are taken up and lost, but it is possible that the combined rate of lateral gene transfer and gene loss is higher than that of point mutation. What evolutionary forces underlie the rate of lateral gene transfer are not well understood. We here use theory developed to explain the evolution of mutation rates to address this question and explore its consequences for the study of prokaryote evolution.