Figure 2 - uploaded by Nobuto Takeuchi
Content may be subject to copyright.
Conceptual diagram of the model. (a) A prokaryotic genome assumed in the model. The box labeled with E indicates a locus involved in adaptation to a new ecological niche (E locus). The boxes labeled with S indicate susceptibility loci subject to NFDS (S loci). The box labeled with N indicates a neutral locus (N locus). (b) The loci and alleles assumed in the model prokaryote genome. E locus, ecological locus; N locus, neutral locus; S loci, susceptibility loci.
Source publication
Background
Fixation of beneficial genes in bacteria and archaea (collectively, prokaryotes) is often believed to erase pre-existing genomic diversity through the hitchhiking effect, a phenomenon known as genome-wide selective sweep. Recent studies, however, indicate that beneficial genes spread through a prokaryotic population via recombination wit...
Contexts in source publication
Context 1
... that a population of prokaryotes is evolving to- ward adaptation to a new ecological niche. The genomes of these prokaryotes are assumed to consist of three types of loci ( Figure 2a): (i) loci involved in the adapta- tion to the new niche (E or ecological loci, for short), (ii) n loci subject to NFDS (S or susceptibility loci, for short), and (iii) all the other loci, which are assumed to be neutral (N or neutral loci, for short; only one such locus is shown in Figure 2a). The S loci assume l alleles per locus, allowing for a total of l n allelic patterns or l n susceptibility types (see Table 1 for notation). ...
Context 2
... that a population of prokaryotes is evolving to- ward adaptation to a new ecological niche. The genomes of these prokaryotes are assumed to consist of three types of loci ( Figure 2a): (i) loci involved in the adapta- tion to the new niche (E or ecological loci, for short), (ii) n loci subject to NFDS (S or susceptibility loci, for short), and (iii) all the other loci, which are assumed to be neutral (N or neutral loci, for short; only one such locus is shown in Figure 2a). The S loci assume l alleles per locus, allowing for a total of l n allelic patterns or l n susceptibility types (see Table 1 for notation). ...
Context 3
... the model considers populations of prokaryotic hosts and vi- ruses. Prokaryotic genomes are assumed to encompass three types of loci (Figure 2b): (i) one E locus that as- sumes either the wild-type or beneficial allele (denoted by 0 and 1, respectively), (ii) n S loci that assume l alleles per locus (which determine susceptibility to viral infec- tion as described later), and (iii) one N locus that as- sumes two neutral alleles (denoted by 0 or 1). For simplicity, the model explicitly incorporates only one N locus to consider the average relative decrease of per- locus neutral diversity caused by a selective sweep (per- locus diversity is more relevant than genotype diversity under the situation in which recombination is a more dominant source of genetic variation than mutations; also, per-locus diversity has been considered in previous work [17]). ...
Citations
... In recent years, microbiome stability and variation have become a major problem in microbiology, with important implications for human health [28,29]. Horizontal gene transfer plays a crucial role in the preservation of genome diversity [30][31][32][33][34][35][36] but the effects of environmental variations on the microbiome composition remain poorly understood. Evolutionary processes in populations in time-varying environments can drastically differ from those in fixed environments [37][38][39][40][41][42][43][44][45][46][47][48]. ...
Microbiomes are generally characterized by high diversity of coexisting microbial species and strains that remains stable within a broad range of conditions. However, under fixed conditions, microbial ecology conforms with the exclusion principle under which two populations competing for the same resource within the same niche cannot coexist because the less fit population inevitably goes extinct. To explore the conditions for stabilization of microbial diversity, we developed a simple mathematical model consisting of two competing populations that could exchange a single gene allele via horizontal gene transfer (HGT). We found that, although in a fixed environment, with unbiased HGT, the system obeyed the exclusion principle, in an oscillating environment, within large regions of the phase space bounded by the rates of reproduction and HGT, the two populations coexist. Moreover, depending on the parameter combination, all three major types of symbiosis obtained, namely, pure competition, host-parasite relationship and mutualism. In each of these regimes, certain parameter combinations provided for synergy, that is, a greater total abundance of both populations compared to the abundance of the winning population in the fixed environments. These findings show that basic phenomena that are universal in microbial communities, environmental variation and HGT, provide for stabilization of microbial diversity and ecological complexity.
... Another mechanisms, put forward by Takeuchi and coworkers in 2015 [23], involves the linkage of the beneficial sweeping gene with widespread (species-specific) deleterious alleles, which would lead to negative frequency-dependent selection. This mechanism was shown to explain a gene-sweep dynamics in quantitative terms, provided that the basal recombination rate, (the spontaneous rate, not affected by selective pressure), is sufficiently low. ...
... This mechanism was shown to explain a gene-sweep dynamics in quantitative terms, provided that the basal recombination rate, (the spontaneous rate, not affected by selective pressure), is sufficiently low. The widespread linkage of the beneficial gene with deleterious alleles or more generally the presence of linked loci under negative frequency-dependent selection, does not have a simple explanation, but the authors speculate that it could be the consequence of ecological interactions between bacteria and viral predators [23], possibly supported by a "Kill the Winner" dynamics [24]. Interestingly, this mechanism can work with relatively low gene-transfer rates, and actually requires a low basal recombination rate. ...
... Apart from these differences, the mechanisms described by our work are conceptually similar to the ones discussed by Niehus and coworkers, in that they are a result of the balance between HGT and migration rates. As noted in ref. [6], these mechanisms lead to an effective frequency-dependent selection (which in our case acts completely at the level of populations within a metacommunity, not on individuals), as it reproduces the same effect defined by Takeuchi and coworkers [23]. However, we note that this dependency has a different origin than the processes hypothesized by Takeuchi and coworkers [23] (which act at the level of an individual within a population). ...
The horizontal transfer of genes is fundamental for the eco-evolutionary dynamics of microbial communities, such as oceanic plankton, soil, and the human microbiome. In the case of an acquired beneficial gene, classic population genetics would predict a genome-wide selective sweep, whereby the genome spreads clonally within the community and together with the beneficial gene, removing genome diversity. Instead, several sources of metagenomic data show the existence of “gene-specific sweeps”, whereby a beneficial gene spreads across a bacterial community, maintaining genome diversity. Several hypotheses have been proposed to explain this process, including the decreasing gene flow between ecologically distant populations, frequency-dependent selection from linked deleterious allelles, and very high rates of horizontal gene transfer. Here, we propose an additional possible scenario grounded in eco-evolutionary principles. Specifically, we show by a mathematical model and simulations that a metacommunity where species can occupy multiple patches, acting together with a realistic (moderate) HGT rate, helps maintain genome diversity. Assuming a scenario of patches dominated by single species, our model predicts that diversity only decreases moderately upon the arrival of a new beneficial gene, and that losses in diversity can be quickly restored. We explore the generic behaviour of diversity as a function of three key parameters, frequency of insertion of new beneficial genes, migration rates and horizontal transfer rates.Our results provides a testable explanation for how diversity can be maintained by gene-specific sweeps even in the absence of high horizontal gene transfer rates.
... On ecological time scales, differences in rates of relative lifetime reproductive success have been measured directly using intensive monitoring/tagging approaches (Goldberg et al., 2020), pedigree analyses (Christie et al., 2018;Fradgley et al., 2019), or indirectly with genetic methods such as calculating the effective number of breeders within each generation (Christie et al., 2012;Luikart et al., 2021). NFDS may also be detectable by identifying signatures of NFDS within and among genomes (Cavedon et al., 2019;Takeuchi et al., 2015). For example, Cavedon et al. (2019) found signatures of balancing selection related to different migratory behaviors among populations of caribou distributed along an environmental cline which, when coupled with strong signals of divergent selection between behavioral types, suggests a role for NFDS. ...
From genes to communities, understanding how diversity is maintained remains a fundamental question in biology. One challenging to identify, yet potentially ubiquitous, mechanism for the maintenance of diversity is negative frequency dependent selection (NFDS), which occurs when entities (e.g., genotypes, life history strategies, species) experience a per capita reduction in fitness with increases in relative abundance. Because NFDS allows rare entities to increase in frequency while preventing abundant entities from excluding others, we posit that negative frequency dependent selection plays a central role in the maintenance of diversity. In this review, we relate NFDS to coexistence, identify mechanisms of NFDS (e.g., mutualism, predation, parasitism), review strategies for identifying NFDS, and distinguish NFDS from other mechanisms of coexistence (e.g., storage effects, fluctuating selection). We also emphasize that NFDS is a key place where ecology and evolution intersect. Specifically, there are many examples of frequency dependent processes in ecology, but fewer cases that link this process to selection. Similarly, there are many examples of selection in evolution, but fewer cases that link changes in trait values to negative frequency dependence. Bridging these two well-developed fields of ecology and evolution will allow for mechanistic insights into the maintenance of diversity at multiple levels.
... A second mechanism, proposed by Niehus and coworkers [6], proposes that the combination of a small migration rate and a high HGT rate can lead to the fixation of beneficial genes without the decrease of genome diversity. A different hypothesis, put forward by Takeuchi and coworkers in 2015 [14], involves the linkage of the beneficial sweeping gene with widespread (species-specific) deleterious alleles, which would lead to negative frequency-dependent selection. This mechanism was shown to explain a gene-sweep dynamics in quantitative terms, provided that the basal recombination rate is sufficiently low. ...
... This mechanism was shown to explain a gene-sweep dynamics in quantitative terms, provided that the basal recombination rate is sufficiently low. The widespread linkage of the beneficial gene with deleterious alleles does not have a simple explanation, but the authors speculate that it could be the consequence of ecological interactions between bacteria and viral predators [14], possibly supported by a "Kill the Winner" dynamics [15]. Finally, a complementary scenario for gene sweeping might be the so-called "soft sweeps" [16,17], where widespread (e.g. ...
... As noted in ref. [6], these mechanisms lead to an effective frequency-dependent selection (which in our case acts completely at the level of populations within a metacommunity, not on individuals). However, we note that this dependency has a different origin than the processes hypothesized by Takeuchi and coworkers [14] (which act at the level of an individual within a population). In the scenario assumed by Takeuchi and colleagues, the diversity is favored by ubiquitous and diverse deleterious loci that are linked to the acquired beneficial gene. ...
The horizontal transfer of genes is fundamental for the eco-evolutionary dynamics of microbial communities, such as oceanic plankton, soil, and the human microbiome. In the case of an acquired beneficial gene, classic population genetics would predict a genome-wide selective sweep, whereby the genome spreads clonally with the gene, removing genome diversity. Instead, several sources of metagenomic data show the existence of "gene-specific sweeps", whereby a beneficial gene spreads across a bacterial community, maintaining genome diversity. Several hypotheses have been proposed to explain this process, including the decreasing gene flow between ecologically distant populations, frequency-dependent selection from linked deleterious alleles, and very high rates of horizontal gene transfer. Here, we propose an additional possible scenario grounded in eco-evolutionary principles. Specifically, we show by a mathematical model and simulations that a metacommunity where species can occupy multiple patches helps maintain genome diversity. Assuming a scenario of patches dominated by single species, our model predicts that diversity only decreases moderately upon the arrival of a new beneficial gene, and that losses in diversity can be quickly restored. We explore the generic behaviour of diversity as a function of three key parameters, frequency of insertion of new beneficial genes, migration rates and horizontal transfer rates.Our results provides a testable explanation for how diversity can be maintained given gene-specific sweeps even in the absence of high horizontal gene transfer rates.
... In contrast to the genome simplification observed in host-dependent and streamlined prokaryotes, genome expansion is expected in free-living lineages that inhabit complex environments like soils or sediments, where microenvironments with strikingly different abiotic conditions can be found millimeters apart [69]. Although temporal diversity declines and sweeps for specific gene variants are likely to occur in soil prokaryotes due to rapidly changing environmental conditions [69,70], larger genomes may be selected in these environmental realms due to variable abiotic and biotic constraints. Indeed, a study exploring the genes enriched in larger genomes of soil prokaryotes found a larger proportion of genes involved in regulation and secondary metabolism, and were depleted in genes related with translation, replication, cell division, and nucleotides metabolism when compared with smaller genomes [60]. ...
The evolutionary forces that determine genome size in bacteria and archaea have been the subject of intense debate over the last few decades. Although the preferential loss of genes observed in prokaryotes is explained through the deletional bias, factors promoting and preventing the fixation of such gene losses often remain unclear. Importantly, statistical analyses on this topic typically do not consider the potential bias introduced by the shared ancestry of many lineages, which is critical when using species as data points because of the potential dependence on residuals. In this study, we investigated the genome size distributions across a broad diversity of bacteria and archaea to evaluate if this trait is phylogenetically conserved at broad phylogenetic scales. After model fit, Pagel’s lambda indicated a strong phylogenetic signal in genome size data, suggesting that the diversification of this trait is influenced by shared evolutionary histories. We used a phylogenetic generalized least-squares analysis (PGLS) to test whether phylogeny influences the predictability of genome size from dN/dS ratios and 16S copy number, two variables that have been previously linked to genome size. These results confirm that failure to account for evolutionary history can lead to biased interpretations of genome size predictors. Overall, our results indicate that although bacteria and archaea can rapidly gain and lose genetic material through gene transfers and deletions, respectively, phylogenetic signal for genome size distributions can still be recovered at broad phylogenetic scales that should be taken into account when inferring the drivers of genome size evolution.
... Second, our data show that Fisher-Muller mechanisms function in recombining populations of microbes and can ameliorate the costs of the horizontal import of deleterious genetic variants in adapting populations. Although H. pylori has an exceptionally high recombination rate (63), the observation of gene-specific sweeps in natural microbiomes (21,64,65) suggests that the two impacts of recombination observed in this study-the introduction and reshuffling of novel genetic variation-are likely to be common in natural microbial populations. Future experimental and theoretical studies need to take horizontal gene flow and recombination into account when considering adaptation in natural and clinical microbial communities. ...
Significance
Horizontal gene transfer (HGT)—the transfer of DNA between lineages—is responsible for a large proportion of the genetic variation that contributes to evolution in microbial populations. While HGT can bring beneficial genetic innovation, the transfer of DNA from other species or strains can also have deleterious effects. In this study, we evolve populations of the bacteria Helicobacter pylori and use DNA sequencing to identify over 40,000 genetic variants transferred by HGT. We measure the cost of many of these and find that both strongly beneficial mutations and deleterious mutations are genetic variants transferred by natural transformation. Importantly, we also show how recombination that separates linked beneficial and deleterious mutations resolves the cost of HGT.
... Evidence of the importance of HGT in APEC comes from the divergent position of strains across the population phylogeny (Fig. 3a), as well as the lower mean consistency index of individual pathogenicity-associated gene trees compared with core genes. This suggests homoplasy and the horizontal spread of adaptive genes through the population, consistent with a genespecific selective sweep, or divided genome, model of bacterial evolution 53,81,82 . In this scenario, as migration from the gut occurs, HGT will increase the rate at which positively selected genes sweep through the invasive population. ...
Chickens are the most common birds on Earth and colibacillosis is among the most common diseases affecting them. This major threat to animal welfare and safe sustainable food production is difficult to combat because the etiological agent, avian pathogenic Escherichia coli (APEC), emerges from ubiquitous commensal gut bacteria, with no single virulence gene present in all disease-causing isolates. Here, we address the underlying evolutionary mechanisms of extraintestinal spread and systemic infection in poultry. Combining population scale comparative genomics and pangenome-wide association studies, we compare E. coli from commensal carriage and systemic infections. We identify phylogroup-specific and species-wide genetic elements that are enriched in APEC, including pathogenicity-associated variation in 143 genes that have diverse functions, including genes involved in metabolism, lipopolysaccharide synthesis, heat shock response, antimicrobial resistance and toxicity. We find that horizontal gene transfer spreads pathogenicity elements, allowing divergent clones to cause infection. Finally, a Random Forest model prediction of disease status (carriage vs. disease) identifies pathogenic strains in the emergent ST-117 poultry-associated lineage with 73% accuracy, demonstrating the potential for early identification of emergent APEC in healthy flocks.
... However, the evolutionary etiology of biological systems is not always fully accessible to us (Ardern, 2018) and sometimes the history of selection in a lineage or for a particular gene may be inaccessible or the accessible parts incomplete in important ways. The genomic influence of different kinds of selection on bacterial genomes, including selective sweeps, background selection, positive selection, and purifying selection, remains a point of contention (Takeuchi et al., 2015;Bendall et al., 2016;Gibson and Eyre-Walker, 2019;Sela et al., 2019). Perhaps the most difficult issue here is how to characterize function in young genes, which may be subject to evolutionary forces lying anywhere along a spectrum between positive selection and purifying selection. ...
Many prokaryotic RNAs are transcribed from loci outside of annotated protein coding genes. Across bacterial species hundreds of short open reading frames antisense to annotated genes show evidence of both transcription and translation, for instance in ribosome profiling data. Determining the functional fraction of these protein products awaits further research, including insights from studies of molecular interactions and detailed evolutionary analysis. There are multiple lines of evidence however that many of these newly discovered proteins are of use to the organism. Condition-specific phenotypes have been characterised for a few. These proteins should be added to genome annotations, and the methods for predicting them standardised. Evolutionary analysis of these typically young sequences also may provide important insights into gene evolution. This research should be prioritised for its exciting potential to uncover large numbers of novel proteins with extremely diverse potential practical uses, including applications in synthetic biology and responding to pathogens.
... It is, however, difficult to clearly quantify the impact of gene flow on genome evolution (Bobay et al. 2015) and a recent experimental evolution study has shown that gene flow can even lead to the extinction of beneficial alleles (Maddamsetti and Lenski 2018). It is possible that additional factors counteract genome sweeps, such as clonal interference (Lieberman et al. 2014;Maddamsetti et al. 2015) and negative frequency-dependent selection (Cordero and Polz 2014;Takeuchi et al. 2015). ...
Species constitute the fundamental units of taxonomy and an ideal species definition would embody groups of genetically cohesive organisms reflecting their shared history, traits, and ecology. In contrast to animals and plants, where genetic cohesion can essentially be characterized by sexual compatibility and population structure, building a biologically relevant species definition remains a challenging endeavor in prokaryotes. Indeed, the structure, ecology, and dynamics of microbial populations are still largely enigmatic, and many aspects of prokaryotic genomics deviate from sexual organisms. In this chapter, I present the main concepts and operational definitions commonly used to designate microbial species. I further emphasize how these different concepts accommodate the idiosyncrasies of prokaryotic genomics, in particular, the existence of a core- and a pangenome. Although prokaryote genomics is undoubtedly different from animals and plants, there is growing evidence that gene flow—similar to sexual reproduction—plays a significant role in shaping the genomic cohesiveness of microbial populations, suggesting that, to some extent, a species definition based on the Biological Species Concept is applicable to prokaryotes. Building a satisfying species definition remains to be accomplished, but the integration of genomic data, ecology, and bioinformatics tools has expanded our comprehension of prokaryotic populations and their dynamics.
... It is, however, difficult to clearly quantify the impact of gene flow on genome evolution (Bobay et al. 2015) and a recent experimental evolution study has shown that gene flow can even lead to the extinction of beneficial alleles (Maddamsetti and Lenski 2018). It is possible that additional factors counteract genome sweeps, such as clonal interference (Lieberman et al. 2014;Maddamsetti et al. 2015) and negative frequency-dependent selection (Cordero and Polz 2014;Takeuchi et al. 2015). ...
The first eukaryotes emerged from their prokaryotic ancestors more than 1.5 billion years ago and rapidly spread over the planet, first in the ocean, later on as land animals, plants, and fungi. Taking advantage of an expanding genome complexity and flexibility, they invaded almost all known ecological niches, adapting their body plan, physiology, and metabolism to new environments. This increase in genome complexity came along with an increase in gene repertoire, mainly from molecular reassortment of existing protein domains, but sometimes from the capture of a piece of viral genome or of a transposon sequence. With increasing sequencing and computing powers, it has become possible to undertake deciphering eukaryotic genome contents to an unprecedented scale, collecting all genes belonging to a given species, aiming at compiling all essential and dispensable genes making eukaryotic life possible.
