Horizontal gene transfer (HGT), the acquisition of genetic material from non-parental lineages, is known to be important in bacterial evolution. In particular, HGT provides rapid access to genetic innovations, allowing traits such as virulence, antibiotic resistance and xenobiotic metabolism to spread through the human microbiome. Recent anecdotal studies providing snapshots of active gene flow on the human body have highlighted the need to determine the frequency of such recent transfers and the forces that govern these events. Here we report the discovery and characterization of a vast, human-associated network of gene exchange, large enough to directly compare the principal forces shaping HGT. We show that this network of 10,770 unique, recently transferred (more than 99% nucleotide identity) genes found in 2,235 full bacterial genomes, is shaped principally by ecology rather than geography or phylogeny, with most gene exchange occurring between isolates from ecologically similar, but geographically separated, environments. For example, we observe 25-fold more HGT between human-associated bacteria than among ecologically diverse non-human isolates (P = 3.0 × 10(-270)). We show that within the human microbiome this ecological architecture continues across multiple spatial scales, functional classes and ecological niches with transfer further enriched among bacteria that inhabit the same body site, have the same oxygen tolerance or have the same ability to cause disease. This structure offers a window into the molecular traits that define ecological niches, insight that we use to uncover sources of antibiotic resistance and identify genes associated with the pathology of meningitis and other diseases.
Genetic exchange is common among bacteria, but its effect on population diversity during ecological differentiation remains controversial. A fundamental question is whether advantageous mutations lead to selection of clonal genomes or, as in sexual eukaryotes, sweep through populations on their own. Here we show that in two recently diverged populations of ocean bacteria, ecological differentiation has occurred akin to a sexual mechanism: a few genome regions have swept through subpopulations in a habitat specific manner, accompanied by gradual separation of gene pools as evidenced by increased habitat-specificity of the most recent recombinations. These findings reconcile previous, seemingly contradictory empirical observations of the genetic structure of bacterial populations, and point to a more unified process of differentiation in bacteria and sexual eukaryotes than previously imagined.
The importance of microbial communities (MCs) cannot be overstated. MCs underpin the biogeochemical cycles of the earth's soil, oceans and the atmosphere, and perform ecosystem functions that impact plants, animals and humans. Yet our ability to predict and manage the function of these highly complex, dynamically changing communities is limited. Building predictive models that link MC composition to function is a key emerging challenge in microbial ecology. Here, we argue that addressing this challenge requires close coordination of experimental data collection and method development with mathematical model building. We discuss specific examples where model–experiment integration has already resulted in important insights into MC function and structure. We also highlight key research questions that still demand better integration of experiments and models. We argue that such integration is needed to achieve significant progress in our understanding of MC dynamics and function, and we make specific practical suggestions as to how this could be achieved.
In the ocean, organic particles harbour diverse bacterial communities, which collectively digest and recycle essential nutrients. Traits like motility and exo-enzyme production allow individual taxa to colonize and exploit particle resources, but it remains unclear how community dynamics emerge from these individual traits. Here we track the taxon and trait dynamics of bacteria attached to model marine particles and demonstrate that particle-attached communities undergo rapid, reproducible successions driven by ecological interactions. Motile, particle-degrading taxa are selected for during early successional stages. However, this selective pressure is later relaxed when secondary consumers invade, which are unable to use the particle resource but, instead, rely on carbon from primary degraders. This creates a trophic chain that shifts community metabolism away from the particle substrate. These results suggest that primary successions may shape particle-attached bacterial communities in the ocean and that rapid community-wide metabolic shifts could limit rates of marine particle degradation.
A common strategy among microbes living in iron-limited environments is the secretion of siderophores, which can bind poorly soluble iron and make it available to cells via active transport mechanisms. Such siderophore-iron complexes can be thought of as public goods that can be exploited by local communities and drive diversification, for example by the evolution of "cheating." However, it is unclear whether bacterial populations in the environment form stable enough communities such that social interactions significantly impact evolutionary dynamics. Here we show that public good games drive the evolution of iron acquisition strategies in wild populations of marine bacteria. We found that within nonclonal but ecologically cohesive genotypic clusters of closely related Vibrionaceae, only an intermediate percentage of genotypes are able to produce siderophores. Nonproducers within these clusters exhibited selective loss of siderophore biosynthetic pathways, whereas siderophore transport mechanisms were retained, suggesting that these nonproducers can act as cheaters that benefit from siderophore producers in their local environment. In support of this hypothesis, these nonproducers in ironlimited media suffer a significant decrease in growth, which can be alleviated by siderophores, presumably owing to the retention of transport mechanisms. Moreover, using ecological data of resource partitioning, we found that cheating coevolves with the ecological specialization toward association with larger particles in the water column, suggesting that these can harbor stable enough communities for dependencies among organisms to evolve. microbial diversity | ocean bacteria | population structure |
Comparisons of closely related microorganisms have shown that individual genomes can be highly diverse in terms of gene content. In this Review, we discuss several studies showing that much of this variation is associated with social and ecological interactions, which have an important role in the population biology of wild populations of bacteria and archaea. These interactions create frequency-dependent selective pressures that can either stabilize gene frequencies at intermediate levels in populations or promote fast gene turnover, which presents as low gene frequencies in genome surveys. Thus, interpretation of gene-content diversity requires the delineation of populations according to cohesive gene flow and ecology, as micro-evolutionary changes arise in response to local selection pressures and population dynamics.
Phosphorothioate (PT) modification of DNA, with sulfur replacing a nonbridging phosphate oxygen, was recently discovered as a product of the dnd genes found in bacteria and archaea. Given our limited understanding of the biological function of PT modifications, including sequence context, genomic frequencies, and relationships to the diversity of dnd gene clusters, we undertook a quantitative study of PT modifications in prokaryotic genomes using a liquid chromatography-coupled tandem quadrupole mass spectrometry approach. The results revealed a diversity of unique PT sequence contexts and three discrete genomic frequencies in a wide range of bacteria. Metagenomic analyses of PT modifications revealed unique ecological distributions, and a phylogenetic comparison of dnd genes and PT sequence contexts strongly supports the horizontal transfer of dnd genes. These results are consistent with the involvement of PT modifications in a type of restriction-modification system with wide distribution in prokaryotes.DNA modification | bioanalytical chemistry | sulfur P hosphorothioate (PT) modification of DNA, in which sulfur replaces a nonbridging phosphate oxygen, was originally developed as an artificial means to stabilize oligodeoxynucleotides against nuclease degradation (1). However, we recently discovered that the dnd gene products incorporate sulfur into the DNA backbone as a PT in a sequence-and stereo-specific manner (2). Beginning with the original observation in Streptomyces lividans 1326 that the five-gene dnd cluster (dndA-E) caused DNA degradation during electrophoresis (3), the presence of dnd genes has been established in dozens of different bacteria and archaea (4). An emerging picture of Dnd protein function reveals that DndA acts as a cysteine desulfurase and assembles DndC as a 4Fe-4S cluster protein (5). DndC possesses ATP pyrophosphatase activity and is predicted to have PAPS reductase activity, whereas DndB has homology to a group of transcriptional regulators (4, 6). A DndD homologue in Pseudomonas fluorescens Pf0-1, SpfD, has ATPase activity possibly related to DNA structure alteration or nicking during PT incorporation (7).This progress in defining the biochemistry of PT modifications belies a lack of understanding of the biological function of PT modifications, such as the variety of sequence contexts, the distribution of modifications across prokaryotic genomes, and the relationship of PT sequence contexts to the diversity of known dnd gene clusters (4). We have approached this problem with a highly quantitative study of PT modifications in prokaryotic genomes using a liquid chromatography-coupled tandem quadrupole mass spectrometry (LC-MS/MS) approach. The results reveal a diversity of quantized PT sequence contexts consistent with a role for PT modifications as part of a restrictionmodification system. Results and DiscussionDevelopment of a Sensitive Method to Quantify PT Modifications in Bacterial Genomes. We approached the problem of defining the biological function of PT modifications by q...
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