Publications
131 results found
Barraclough T, Culbert C, O'Brien S, 2023, Community composition drives siderophore dynamics in multispecies bacterial communities, BMC Ecology and Evolution, Vol: 23, Pages: 1-9, ISSN: 2730-7182
BackgroundIntraspecific public goods are commonly shared within microbial populations, where the benefits of public goods are largely limited to closely related conspecifics. One example is the production of iron-scavenging siderophores that deliver iron to cells via specific cell envelope receptor and transport systems. Intraspecific social exploitation of siderophore producers is common, since non-producers avoid the costs of production but retain the cell envelope machinery for siderophore uptake. However, little is known about how interactions between species (i.e., interspecific interactions) can shape intraspecific public goods exploitation. Here, we predicted that strong competition for iron between species in diverse communities will increase costs of siderophore cooperation, and hence drive intraspecific exploitation. We examined how increasing microbial community species diversity shapes intraspecific social dynamics by monitoring the growth of siderophore producers and non-producers of the plant-growth promoting bacterium Pseudomonas fluorescens, embedded within tree-hole microbial communities ranging from 2 to 15 species.ResultsWe find, contrary to our prediction, that siderophore production is favoured at higher levels of community species richness, driven by increased likelihood of encountering key species that reduce the growth of siderophore non-producing (but not producing) strains of P. fluorescens.ConclusionsOur results suggest that maintaining a diverse soil microbiota could partly contribute to the maintenance of siderophore production in natural communities.
Wu J, Zhang H, Gan R, et al., 2023, CRISPR dynamics during the interaction between bacteria and phage in the first year of life., Microb Genom, Vol: 9
Gut microbiomes in infancy have a profound impact on health in adulthood. CRISPRs play an essential role in the interaction between bacteria and phages. However, the dynamics of CRISPRs in gut microbiomes during early life are poorly understood. In this study, using shotgun metagenomic sequencing data from 82 Swedish infants' gut microbiomes, 1882 candidate CRISPRs were identified, and their dynamics were analysed. We found large-scale turnover of CRISPRs and their spacers during the first year of life. As well as changes in relative abundance of the bacteria containing CRISPR, acquisition, loss and mutation of spacers were observed within the same CRISPR array sampled over time. Accordingly, the inferred interaction network of bacteria and phage was distinct at different times. This research underpins CRISPR dynamics and their potential role in the interaction between bacteria and phage in early life.
Barraclough T, Peck L, Zhang X, et al., 2023, Temperature contributes to host specialization of coffee wilt disease (Fusarium xylarioides) on arabica and robusta coffee crops, Scientific Reports, Vol: 13, Pages: 1-12, ISSN: 2045-2322
Coffee wilt disease, caused by the fungus Fusarium xylarioides, is a vascular wilt disease that has affected coffee production in sub-Saharan Africa over the past century. Today, the disease has two host-specific populations specialising on arabica and robusta coffee crops, which grow at high and low altitude, respectively. Here we test whether adaptation to different temperatures contributes to specialisation of the fungi on each crop. Firstly, climate models show that the severity of the arabica and robusta populations of coffee wilt disease correlates with temperature. The robusta population shows higher peak severity than the arabica population overall, but the latter has greater cold tolerance. Secondly, growth assays of thermal performance of fungal strains in vitro show that, while robusta strains grow faster than arabicas at intermediate temperatures, the arabica strains have higher sporulation and spore germination rates at temperatures below 15ºC. The match between environmental patterns of severity in nature with thermal performance of fungal cultures in the laboratory supports a role for temperature adaptation in specialisation on arabica and robusta coffee. Extrapolating our temperature-models to future climate change predicts that disease severity could decline on average due to increased temperature but could increase in some coffee-growing regions.
Barraclough T, Llewellyn T, Nowell R, et al., 2023, Metagenomics shines light on the evolution of ‘sunscreen’ pigment metabolism in the Teloschistales (lichen-forming Ascomycota), Genome Biology and Evolution, Vol: 15, Pages: 1-19, ISSN: 1759-6653
Fungi produce a vast number of secondary metabolites that shape their interactions with other organisms and the environment. Characterizing the genes underpinning metabolite synthesis is therefore key to understanding fungal evolution and adaptation. Lichenized fungi represent almost one-third of Ascomycota diversity and boast impressive secondary metabolites repertoires. However, most lichen biosynthetic genes have not been linked to their metabolite products. Here we used metagenomic sequencing to survey gene families associated with production of anthraquinones, UV-protectant secondary metabolites present in various fungi, but especially abundant in a diverse order of lichens, the Teloschistales (class Lecanoromycetes, phylum Ascomycota). We successfully assembled 24 new, high-quality lichenized-fungal genomes de novo and combined them with publicly available Lecanoromycetes genomes from taxa with diverse secondary chemistry to produce a whole-genome tree. Secondary metabolite biosynthetic gene cluster (BGC) analysis showed that whilst lichen BGCs are numerous and highly dissimilar, core enzyme genes are generally conserved across taxa. This suggests metabolite diversification occurs via re-shuffling existing enzyme genes with novel accessory genes rather than BGC gains/losses or de novo gene evolution. We identified putative anthraquinone BGCs in our lichen dataset that appear homologous to anthraquinone clusters from non-lichenized fungi, suggesting these genes were present in the common ancestor of the subphylum Pezizomycotina. Finally, we identified unique transporter genes in Teloschistales anthraquinone BGCs that may explain why these metabolites are so abundant and ubiquitous in these lichens. Our results support the importance of metagenomics for understanding the secondary metabolism of non-model fungi such as lichens.
Ryan MJ, Peck LD, Smith D, et al., 2022, Culture collections as a source of historic strains for genomic studies in plant pathology, JOURNAL OF PLANT PATHOLOGY, ISSN: 1125-4653
Lu M, Fradera-Soler M, Forest F, et al., 2022, Evidence linking life-form to a major shift in diversification rate in Crassula, AMERICAN JOURNAL OF BOTANY, Vol: 109, Pages: 272-290, ISSN: 0002-9122
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- Citations: 2
Scheuerl T, Hopkins M, Nowell RW, et al., 2021, Bacterial adaptation is constrained in complex communities (vol 11, 754, 2021), NATURE COMMUNICATIONS, Vol: 12
Sheppard RJ, Barraclough TG, Jansen VAA, 2021, The evolution of plasmid transfer rate in bacteria and its effect on plasmid persistence, The American Naturalist, Vol: 198, Pages: 473-488, ISSN: 0003-0147
Plasmids are extrachromosomal segments of DNA that can transfer genes between bacterial cells. Many plasmid genes benefit bacteria but cause harm to human health by granting antibiotic resistance to pathogens. Transfer rate is a key parameter for predicting plasmid dynamics, but observed rates are highly variable, and the effects of selective forces on their evolution are unclear. We apply evolutionary analysis to plasmid conjugation models to investigate selective pressures affecting plasmid transfer rate, emphasizing host versus plasmid control, the costs of plasmid transfer, and the role of recipient cells. Our analyses show that plasmid-determined transfer rates can be predicted with three parameters (host growth rate, plasmid loss rate, and the cost of plasmid transfer on growth) under some conditions. We also show that low-frequency genetic variation in transfer rate can accumulate, facilitating rapid adaptation to changing conditions. Furthermore, reduced transfer rates due to host control have limited effects on plasmid prevalence until low enough to prevent plasmid persistence. These results provide a framework to predict plasmid transfer rate evolution in different environments and demonstrate the limited impact of host mechanisms to control the costs incurred when plasmids are present.
Nowell RW, Barraclough TG, Wilson CG, 2021, Bdelloid rotifers use hundreds of horizontally acquired genes against fungal pathogens
<jats:title>Abstract</jats:title><jats:p>Obligately asexual lineages are typically rare and short-lived. According to one hypothesis, they adapt too slowly to withstand relentlessly coevolving pathogens. Bdelloid rotifers seem to have avoided this fate, by enduring millions of years without males or sex. We investigated whether bdelloids’ unusual capacity to acquire non-metazoan genes horizontally has enhanced their resistance to pathogens. We found that horizontally transferred genes are three times more likely than native genes to be upregulated in response to a natural fungal pathogen. This enrichment was twofold stronger than that elicited by a physical stressor (desiccation), and the genes showed little overlap. Among hundreds of upregulated non-metazoan genes were RNA ligases putatively involved in resisting fungal toxins and glucanases predicted to bind to fungal cell walls, acquired from bacteria. Our results provide evidence that bdelloids mitigate a predicted challenge of long-term asexuality in part through their ability to acquire and deploy so many foreign genes.</jats:p>
Wu J, Barraclough TG, 2021, CRISPRs are associated with bacterial expansion in the human gut during the first year of life
<jats:title>Abstract</jats:title><jats:p>The dynamics of the gut microbiome in infancy have a profound impact on health in adulthood, but the ecological mechanism underlying the dynamics between bacteria and bacteriophages remains poorly understood. CRISPR is a bacterial adaptive immune system to resist bacteriophages; however, the role they play in the dynamics in infants’ gut microbiota is unknown. In this work, using large-scale metagenomic sequencing data from 82 Sweden infants’ gut microbiomes, 1882 candidate CRISPRs were identified and their dynamics were analyzed. The results showed CRISPRs were distributed in dominant bacteria and could target distinct bacteriophages at different time points with largely alternated spacers. In the putative identical CRISPRs, we found the CRISPRs could acquire new spacers and loss old spacers during the first year. In addition, it is the first time to report that gender was a major factor to determine the bacterial richness and the number of CRISPRs and host range of bacteriophages was narrow <jats:italic>in silico</jats:italic>. Therefore, we concluded that CRISPRs were associated with bacterial expansion. This work improves the understanding of the ecological mechanism behind dynamics in the early life of the human gut and substantially expands the repertoire of predicted CRISPRs providing a resource to study the function of bacterial unknown genes and to enhance the performance of these beneficial bacteria by CRISPR gene-editing technology.</jats:p>
Matthews A, Majeed A, Barraclough TG, et al., 2021, Function is a better predictor of plant rhizosphere community membership than 16S phylogeny, ENVIRONMENTAL MICROBIOLOGY, Vol: 23, Pages: 6089-6103, ISSN: 1462-2912
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- Citations: 1
Barraclough T, Peck L, Nowell R, 2021, Historical genomics reveals the evolutionary mechanisms behind multiple outbreaks of the host-specific coffee wilt pathogen Fusarium xylarioides, BMC Genomics, Vol: 22, ISSN: 1471-2164
Background:Nearly 50% of crop yields are lost to pests and disease, with plants and pathogens locked in an amplified co-evolutionary process of disease outbreaks. Coffee wilt disease, caused by Fusarium xylarioides, decimated coffee production in west and central Africa following its initial outbreak in the 1920s. After successful management, it later re-emerged and by the 2000s comprised two separate epidemics on arabica coffee in Ethiopia and robusta coffee in east and central Africa.Results:Here, we use genome sequencing of six historical culture collection strains spanning 52 years to identify the evolutionary processes behind these repeated outbreaks. Phylogenomic reconstruction using 13,782 single copy orthologs shows that the robusta population arose from the initial outbreak, whilst the arabica population is a divergent sister clade to the other strains. A screen for putative effector genes involved in pathogenesis shows that the populations have diverged in gene content and sequence mainly by vertical processes within lineages. However, 15 putative effector genes show evidence of horizontal acquisition, with close homology to genes from F. oxysporum. Most occupy small regions of homology within wider scaffolds, whereas a cluster of four genes occupy a 20Kb scaffold with strong homology to a region on a mobile pathogenicity chromosome in F. oxysporum that houses known effector genes. Lacking a match to the whole mobile chromosome, we nonetheless found close associations with DNA transposons, especially the miniature impala type previously proposed to facilitate horizontal transfer of pathogenicity genes in F. oxysporum. These findings support a working hypothesis that the arabica and robusta populations partly acquired distinct effector genes via transposition-mediated horizontal transfer from F. oxysporum, which shares coffee as a host and lives on other plants intercropped with coffee.Conclusion:Our results show how historical genomics can help reveal mech
Nowell RW, Wilson CG, Almeida P, et al., 2021, Evolutionary dynamics of transposable elements in bdelloid rotifers, eLife, Vol: 10, Pages: 1-37, ISSN: 2050-084X
Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates in which males are thus far unknown. Contrary to expectations, we find a variety of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms. Instead, we find that that TE content evolves relatively slowly in bdelloids and that gene families involved in RNAi-mediated TE suppression have undergone significant expansion, which might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.
Kontopoulos D-G, Smith TP, Barraclough TG, et al., 2020, Adaptive evolution shapes the present-day distribution of the thermal sensitivity of population growth rate, PLoS Biology, Vol: 18, ISSN: 1544-9173
Developing a thorough understanding of how ectotherm physiology adapts to different thermal environments is of crucial importance, especially in the face of global climate change. A key aspect of an organism's thermal performance curve (TPC)-the relationship between fitness-related trait performance and temperature-is its thermal sensitivity, i.e., the rate at which trait values increase with temperature within its typically experienced thermal range. For a given trait, the distribution of thermal sensitivities across species, often quantified as "activation energy" values, is typically right-skewed. Currently, the mechanisms that generate this distribution are unclear, with considerable debate about the role of thermodynamic constraints versus adaptive evolution. Here, using a phylogenetic comparative approach, we study the evolution of the thermal sensitivity of population growth rate across phytoplankton (Cyanobacteria and eukaryotic microalgae) and prokaryotes (bacteria and archaea), 2 microbial groups that play a major role in the global carbon cycle. We find that thermal sensitivity across these groups is moderately phylogenetically heritable, and that its distribution is shaped by repeated evolutionary convergence throughout its parameter space. More precisely, we detect bursts of adaptive evolution in thermal sensitivity, increasing the amount of overlap among its distributions in different clades. We obtain qualitatively similar results from evolutionary analyses of the thermal sensitivities of 2 physiological rates underlying growth rate: net photosynthesis and respiration of plants. Furthermore, we find that these episodes of evolutionary convergence are consistent with 2 opposing forces: decrease in thermal sensitivity due to environmental fluctuations and increase due to adaptation to stable environments. Overall, our results indicate that adaptation can lead to large and relatively rapid shifts in thermal sensitivity, especially in microbes f
Kontopoulos D-G, Patmanidis I, Barraclough TG, et al., 2020, Higher temperatures worsen the effects of mutations on protein stability
<jats:title>Abstract</jats:title><jats:p>Understanding whether and how temperature increases alter the effects of mutations on protein stability is crucial for understanding the limits to thermal adaptation by organisms. Currently, it is generally assumed that the stability effects of mutations are independent of temperature. Yet, mutations should become increasingly destabilizing as temperature rises due to the increase in the energy of atoms. Here, by performing an extensive computational analysis on the essential enzyme adenylate kinase in prokaryotes, we show, for the first time, that mutations become more destabilizing with temperature both across and within species. Consistent with these findings, we find that substitution rates of prokaryotes decrease nonlinearly with temperature. Our results suggest that life on Earth likely originated in a moderately thermophilic and thermally fluctuating environment, and indicate that global warming should decrease the per-generation rate of molecular evolution of prokaryotes.</jats:p>
Pathak A, Nowell RW, Wilson CG, et al., 2020, Comparative genomics of Alexander Fleming's original Penicillium isolate (IMI 15378) reveals sequence divergence of penicillin synthesis genes, Scientific Reports, Vol: 10, ISSN: 2045-2322
Antibiotics were derived originally from wild organisms and therefore understanding how these compounds evolve among different lineages might help with the design of new antimicrobial drugs. We report the draft genome sequence of Alexander Fleming's original fungal isolate behind the discovery of penicillin, now classified as Penicillium rubens Biourge (1923) (IMI 15378). We compare the structure of the genome and genes involved in penicillin synthesis with those in two 'high producing' industrial strains of P. rubens and the closely related species P. nalgiovense. The main effector genes for producing penicillin G (pcbAB, pcbC and penDE) show amino acid divergence between the Fleming strain and both industrial strains, whereas a suite of regulatory genes are conserved. Homologs of penicillin N effector genes cefD1 and cefD2 were also found and the latter displayed amino acid divergence between the Fleming strain and industrial strains. The draft assemblies contain several partial duplications of penicillin-pathway genes in all three P. rubens strains, to differing degrees, which we hypothesise might be involved in regulation of the pathway. The two industrial strains are identical in sequence across all effector and regulatory genes but differ in duplication of the pcbAB-pcbC-penDE complex and partial duplication of fragments of regulatory genes. We conclude that evolution in the wild encompassed both sequence changes of the effector genes and gene duplication, whereas human-mediated changes through mutagenesis and artificial selection led to duplication of the penicillin pathway genes.
Nowell RW, Wilson CG, Almeida P, et al., 2020, Evolutionary dynamics of transposable elements in bdelloid rotifers
<jats:title>Abstract</jats:title><jats:p>Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates where males are thus far unknown. Contrary to expectations, we find a diverse range of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms, but we report that bdelloids share a large and unusual expansion of genes involved in RNAi-mediated TE suppression. This suggests that enhanced cellular defence mechanisms might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.</jats:p>
Schley RJ, Pennington RT, Perez-Escobar OA, et al., 2020, Introgression across evolutionary scales suggests reticulation contributes to Amazonian tree diversity, MOLECULAR ECOLOGY, Vol: 29, Pages: 4170-4185, ISSN: 0962-1083
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- Citations: 14
Kontopoulos D, van Sebille E, Lange M, et al., 2020, Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints, Evolution, Vol: 74, Pages: 775-790, ISSN: 0014-3820
To better predict how populations and communities respond to climatic temperature variation, it is necessary to understand how the shape of the response of fitness‐related rates to temperature evolves (the thermal performance curve). Currently, there is disagreement about the extent to which the evolution of thermal performance curves is constrained. One school of thought has argued for the prevalence of thermodynamic constraints through enzyme kinetics, whereas another argues that adaptation can—at least partly—overcome such constraints. To shed further light on this debate, we perform a phylogenetic meta‐analysis of the thermal performance curves of growth rate of phytoplankton—a globally important functional group—, controlling for environmental effects (habitat type and thermal regime). We find that thermodynamic constraints have a minor influence on the shape of the curve. In particular, we detect a very weak increase of maximum performance with the temperature at which the curve peaks, suggesting a weak “hotter‐is‐better” constraint. Also, instead of a constant thermal sensitivity of growth across species, as might be expected from strong constraints, we find that all aspects of the thermal performance curve evolve along the phylogeny. Our results suggest that phytoplankton thermal performance curves adapt to thermal environments largely in the absence of hard thermodynamic constraints.
Sheppard R, Beddis A, Barraclough T, 2020, The role of hosts, plasmids and environment in determining plasmid transfer rates: a meta-analysis, Plasmid, Vol: 108, ISSN: 0147-619X
Plasmids transfer at highly variable rates which spread over 10 orders of magnitude. While rates have been measured for decades and it is known that the rates are affected by biotic and abiotic factors, it is unclear how and to what extent these factors determine the rates of transfer. We performed a meta-analysis of 1224 published transfer rates from 33 papers (filtered to 612 transfer rates) to assess this variation. Over three quarters of the variation can be predicted, with plasmid repression and media type (solid versus liquid) identified as general variables explaining the most variation. Of the host and plasmid identities, identity of the recipient bacterium explained the most variation, up to 34% in some models, and more than any other explanatory variable. These results emphasize the role of the recipient in determining the rate of transfer, and show an improved range of transfer values and their correlates that can be used in future when modeling plasmid persistence.
Scheuerl T, Hopkins M, Nowell R, et al., 2020, Bacterial adaptation is constrained in complex communities, Nature Communications, Vol: 11, ISSN: 2041-1723
A major unresolved question is how bacteria living in complex communities respond to environmental changes. In communities, biotic interactions may either facilitate or constrain evolution depending on whether the interactions expand or contract the range of ecological opportunities. A fundamental challenge is to understand how the surrounding biotic community modifies evolutionary trajectories as species adapt to novel environmental conditions. Here we show that community context can dramatically alter evolutionary dynamics using a novel approach that ‘cages’ individual focal strains within complex communities. We find that evolution of focal bacterial strains depends on properties both of the focal strain and of the surrounding community. In particular, there is a stronger evolutionary response in low-diversity communities, and when the focal species have a larger genome and are initially poorly adapted. We see how community context affects resource usage and detect genetic changes involved in carbon metabolism and inter-specific interaction. The findings demonstrate that adaptation to new environmental conditions should be investigated in the context of interspecific interactions.
Schley RJ, Pennington RT, Pérez-Escobar OA, et al., 2019, Introgression across evolutionary scales suggests reticulation contributes to Amazonian tree diversity
<jats:title>Abstract</jats:title><jats:p>Hybridization has the potential to generate or homogenize biodiversity and is a particularly common phenomenon in plants, with an estimated 25% of species undergoing inter-specific gene flow. However, hybridization in Amazonia’s megadiverse tree flora was assumed to be extremely rare despite extensive sympatry between closely related species, and its role in diversification remains enigmatic because it has not yet been examined empirically. Using members of a dominant Amazonian tree family (<jats:italic>Brownea</jats:italic>, Fabaceae) as a model to address this knowledge gap, our study recovered extensive evidence of hybridization among multiple lineages across phylogenetic scales. More specifically, our results uncovered several historical introgression events between<jats:italic>Brownea</jats:italic>lineages and indicated that gene tree incongruence in<jats:italic>Brownea</jats:italic>is best explained by introgression, rather than solely by incomplete lineage sorting. Furthermore, investigation of recent hybridization using ∼19,000 ddRAD loci recovered a high degree of shared variation between two<jats:italic>Brownea</jats:italic>species which co-occur in the Ecuadorian Amazon. Our analyses also showed that these sympatric lineages exhibit homogeneous rates of introgression among loci relative to the genome-wide average, implying a lack of selection against hybrid genotypes and a persistence of hybridization over time. Our results demonstrate that gene flow between multiple Amazonian tree species has occurred across temporal scales, and contrasts with the prevailing view of hybridization’s rarity in Amazonia. Overall, our results provide novel evidence that reticulate evolution influenced diversification in part of the Amazonian tree flora, which is the most diverse on Earth.</jats:p>
Barraclough T, 2019, Species matter for predicting the functioning of evolving microbial communities – an eco-evolutionary model, PLoS ONE, Vol: 14, ISSN: 1932-6203
Humans depend on microbial communities for numerous ecosystem services such as global nutrient cycles, plant growth and their digestive health. Yet predicting dynamics and functioning of these complex systems is hard, making interventions to enhance functioning harder still. One simplifying approach is to assume that functioning can be predicted from the set of enzymes present in a community. Alternatively, ecological and evolutionary dynamics of species, which depend on how enzymes are packaged among species, might be vital for predicting community functioning. I investigate these alternatives by extending classical chemostat models of bacterial growth to multiple species that evolve in their use of chemical resources. Ecological interactions emerge from patterns of resource use, which change as species evolve in their allocation of metabolic enzymes. Measures of community functioning derive in turn from metabolite concentrations and bacterial density. Although the model shows considerable functional redundancy, species packaging does matter by introducing constraints on whether enzyme levels can reach optimum levels for the whole system. Evolution can either promote or reduce functioning compared to purely ecological models, depending on the shape of trade-offs in resource use. The model provides baseline theory for interpreting emerging data on evolution and functioning in real bacterial communities.
Kontopoulos D-G, Smith TP, Barraclough TG, et al., 2019, Adaptive evolution shapes the present-day distribution of the thermal sensitivity of population growth rate
<jats:title>Abstract</jats:title><jats:p>Developing a thorough understanding of how ectotherm physiology adapts to different thermal environments is of crucial importance, especially in the face of global climate change. A key aspect of an organism’s thermal performance curve—the relationship between fitness-related trait performance and temperature—is its thermal sensitivity, i.e., the rate at which trait values increase with temperature within its typically-experienced thermal range. For a given trait, the distribution of thermal sensitivities across species, often quantified as “activation energy” values, is typically right-skewed. Currently, the mechanisms that generate this distribution are unclear, with considerable debate about the role of thermodynamic constraints vs adaptive evolution. Here, using a phylogenetic comparative approach, we study the evolution of the thermal sensitivity of population growth rate across phytoplankton (Cyanobacteria and eukaryotic microalgae) and prokaryotes (bacteria and archaea), two microbial groups that play a major role in the global carbon cycle. We find that thermal sensitivity across these groups is moderately phylogenetically heritable, and that its distribution is shaped by repeated evolutionary convergence throughout its parameter space. More precisely, we detect bursts of adaptive evolution in thermal sensitivity, increasing the amount of overlap among its distributions in different clades. We obtain qualitatively similar results from evolutionary analyses of the thermal sensitivities of two physiological rates underlying growth rate: net photosynthesis and respiration of plants. Furthermore, we find that these episodes of evolutionary convergence are consistent with two opposing forces: decrease in thermal sensitivity due to environmental fluctuations and increase due to adaptation to stable environments. Overall, our results indicate that adaptation can lead to large a
Barraclough TG, 2019, Species matter for predicting the functioning of evolving microbial communities
<jats:title>ABSTRACT</jats:title><jats:p>Humans depend on microbial communities for numerous ecosystem services such as global nutrient cycles, plant growth and their digestive health. Yet predicting dynamics and functioning of these complex systems is hard, making interventions to enhance functioning harder still. One simplifying approach is to assume that functioning can be predicted from the set of enzymes present in a community. Alternatively, ecological and evolutionary dynamics of species, which depend on how enzymes are packaged among species, might be vital for predicting community functioning. I investigate these alternatives by extending classical chemostat models of bacterial growth to multiple species that evolve in their use of chemical resources. Ecological interactions emerge from patterns of resource use, which change as species evolve in their allocation of metabolic enzymes. Measures of community functioning derive in turn from metabolite concentrations and bacterial density. Although the model shows considerable functional redundancy, species packaging does matter by introducing constraints on whether enzyme levels can reach optimum levels for the whole system. Evolution can either promote or reduce functioning compared to purely ecological models, depending on the shape of trade-offs in resource use. The model provides baseline theory for interpreting emerging data on evolution and functioning in real bacterial communities.</jats:p>
Schmutzer M, Barraclough T, 2019, The role of recombination, niche‐specific gene pools and flexible genomes in the ecological speciation of bacteria, Ecology and Evolution, Vol: 9, Pages: 4544-4556, ISSN: 2045-7758
Bacteria diversify into genetic clusters analogous to those observed in sexual eukaryotes, but the definition of bacterial species is an ongoing problem. Recent work has focused on adaptation to distinct ecological niches as the main driver of clustering, but there remains debate about the role of recombination in that process. One view is that homologous recombination occurs too rarely for gene flow to constrain divergent selection. Another view is that homologous recombination is frequent enough in many bacterial populations that barriers to gene flow are needed to permit divergence. Niche-specific gene pools have been proposed as a general mechanism to limit gene flow. We use theoretical models to evaluate additional hypotheses that evolving genetic architecture, specifically the effect sizes of genes and gene gain and loss, can limit gene flow between diverging populations. Our model predicts that i) in the presence of gene flow and recombination, ecological divergence is concentrated in few loci of large effect, and ii) high rates of gene flow plus recombination promote gene loss and favor the evolution of niche-specific genes. The results show that changing genetic architecture and gene loss can facilitate ecological divergence, even without niche-specific gene pools. We discuss these results in the context of recent studies of sympatric divergence in microbes.
Kontopoulos D-G, van Sebille E, Lange M, et al., 2018, Phytoplankton thermal responses adapt in the absence of hard thermodynamic constraints
<jats:title>Abstract</jats:title><jats:p>To better predict how populations and communities respond to climatic temperature variation, it is necessary to understand how the shape of the response of fitness-related traits to temperature evolves (the thermal performance curve). Currently, there is disagreement about the extent to which the evolution of thermal performance curves is constrained. One school of thought has argued for the prevalence of thermodynamic constraints through enzyme kinetics, whereas another argues that adaptation can—at least partly—overcome such constraints. To shed further light on this debate, we perform a phylogenetic meta-analysis of the thermal performance curves of growth rate of phytoplankton—a globally important functional group—, controlling for environmental effects (habitat type and thermal regime). We find that thermodynamic constraints have a minor influence on the shape of the curve. In particular, we detect a very weak increase of maximum performance with the temperature at which the curve peaks, suggesting a weak “hotter-is-better” constraint. Also, instead of a constant thermal sensitivity of growth across species, as might be expected from strong constraints, we find that all aspects of the thermal performance curve evolve along the phylogeny. Our results suggest that phytoplankton thermal performance curves adapt to thermal environments largely in the absence of hard thermodynamic constraints.</jats:p>
Schley RJ, de la Estrella M, Pérez-Escobar OA, et al., 2018, Is Amazonia a ‘museum’ for Neotropical trees? The evolution of the Brownea clade (Detarioideae, Leguminosae), Molecular Phylogenetics and Evolution, Vol: 126, Pages: 279-292, ISSN: 1055-7903
The flora of the Neotropics is unmatched in its diversity, however the mechanisms by which diversity has accumulated are debated and largely unclear. The Brownea clade (Leguminosae) is a characteristic component of the Neotropical flora, and the species within it are diverse in their floral morphology, attracting a wide variety of pollinators. This investigation aimed to estimate species divergence times and infer relationships within the group, in order to test whether the Brownea clade followed the ‘cradle’ or ‘museum’ model of diversification, i.e. whether species evolved rapidly over a short time period, or gradually over many millions of years. We also aimed to trace the spatio-temporal evolution of the clade by estimating ancestral biogeographical patterns in the group. We used BEAST to build a dated phylogeny of 73 Brownea clade species using three molecular markers (ITS, trnK and psbA-trnH), resulting in well-resolved phylogenetic relationships within the clade, as well as robust divergence time estimates from which we inferred diversification rates and ancestral biogeography. Our analyses revealed an Eocene origin for the group, after which the majority of diversification happened in Amazonia during the Miocene, most likely concurrent with climatic and geological changes caused by the rise of the Andes. We found no shifts in diversification rate over time, suggesting a gradual accumulation of lineages with low extinction rates. These results may help to understand why Amazonia is host to the highest diversity of tree species on Earth.
Wilson CG, Nowell R, Barraclough T, 2018, Cross-contamination explains "inter- and intraspecific horizontal genetic transfers" between asexual bdelloid rotifers, Current Biology, Vol: 28, Pages: 2436-2444.e14, ISSN: 1879-0445
A few metazoan lineages are thought to have persisted for millions of years without sexual reproduction. If so, they would offer important clues to the evolutionary paradox of sex itself [1, 2]. Most "ancient asexuals" are subject to ongoing doubt because extant populations continue to invest 17 in males [3–9]. However, males are famously unknown in bdelloid rotifers, a class of microscopic invertebrates comprising hundreds of species [10–12]. Bdelloid genomes have acquired an unusually high proportion of genes from non-metazoans via horizontal transfer [13–17]. This well-substantiated finding has invited speculation [13] that homologous horizontal transfer between bdelloid individuals also may occur, perhaps even "replacing" sex [14]. In 2016, Current Biology published an Article claiming to supply evidence for this idea. Debortoli et al. [18] sampled rotifers from natural populations and sequenced one mitochondrial and four nuclear loci. Species assignments were incongruent among loci for several samples, which was interpreted as evidence of "interspecific horizontal genetic transfers". Here, we use sequencing chromatograms supplied by the authors to demonstrate that samples treated as individuals actually contained two or more highly divergent mitoc hondrial and ribosomal sequences, revealing cross-contamination with DNA from multiple animals of different species. Other chromatograms indicate contamination with DNA from conspecific animals, explaining genetic and genomic evidence for "intraspecific horizontal exchanges" reported in the same study. Given the clear evidence of contamination, the data and findings of Debortoli et al. [18] provide no reliable support for their conclusions that DNA is transferred horizontally between or within bdelloid species.
Barraclough TG, Nowell R, Wilson C, et al., 2018, Comparative genomics of bdelloid rotifers: insights from desiccating and nondesiccating species, PLoS Biology, Vol: 16, ISSN: 1544-9173
Bdelloid rotifers are a Class of microscopic invertebrates that have existed for millions of years apparently without sex or meiosis. They inhabit a variety of temporary and permanent freshwater habitats globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an opportunity to better understand the evolution of sex and recombination, but previous work has emphasized desiccation as the cause of several unusual genomic features in this group. Here, we present high-quality whole genome sequences of three bdelloid species: Rotaria macrura and Rotaria magnacalcarata, which are both desiccation intolerant, and Adineta ricciae, which is desiccationtolerant. In combination with the published assembly of Adineta vaga, which is also desiccation tolerant, we apply a comparative genomics approach to evaluate the potential effects of desiccation tolerance and asexuality on genome evolution in bdelloids. We find that ancestral tetraploidy is conserved among all four bdelloid species, but homologous divergence in obligately aquatic Rotaria genomes is unexpectedly low. This finding is contrary to current models regarding the role of desiccation in shaping bdelloid genomes. In addition, we find that homologous regions in A. ricciaeare largely collinear and do not form palindromic repeats as observed in the published A. vaga assembly. Consequently, several features interpreted as genomic evidence for long-term ameiotic evolution are not general to all bdelloid species, even within the same genus. Finally, we substantiate previous 50 findings of high levels of horizontally transferred non-metazoan genes in both desiccating and non-desiccating bdelloid species, and show that this unusual feature is not shared by other animal phyla, even those with desiccation-tolerant representatives. These comparisons call
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