Biology subjects

Heath, K.

Publications and source records attributed to Heath, K..

12 recordsLinked to original sources

bioRxiv2026

Mutualisms as engines for rapid adaptation: Rhizobium evolution facilitates plant drought resistance

Mutualisms play critical roles in organismal stress tolerance; yet environmental stressors may simultaneously alter the evolution of the mutualism itself. Stress may have particularly strong impacts on the evolution of microbial mutualists due to their capacity for rapid genetic change. Here we used a legume-rhizobia mutualism, in which plants exchange carbon for symbiotically fixed nitrogen, to evaluate how mutualisms evolve in response to stressors. We experimentally evolved populations of Rhizobium leguminasarum in a full factorial design, manipulating drought and nitrogen. We quantified genomic changes in Rhizobium populations as well as their quality as partners with their plant host, Trifolium repens. Drought selected for context- dependent stress benefits to the host; drought-adapted Rhizobium strains provided increased benefits to the host under drought, but fewer benefits to the host in well-watered environments. Conversely, nitrogen fertilization selected for decreased Rhizobium partner quality. Comparative genomics indicated that selection on standing structural variants along the symbiotic plasmid may underpin these drought benefits, specifically along genes associated with desiccation tolerance. These results suggest that stress can expand the benefits rhizobia provide to their legume hosts beyond nitrogen fixation, with rapid symbiont evolution an engine in promoting adaptive plant phenotypes. SIGNIFICANCE STATEMENTWhile mutualisms are fundamental to ecosystem functioning, they are often assumed to break down under environmental stress. We showed the opposite can happen. Here, we factorially manipulated drought stress and nitrogen fertilization and experimentally evolved a model legume-rhizobia mutualism, where rhizobial-bacteria trade nitrogen for plant carbon. When droughted, the symbiotic bacteria rapidly evolved new traits that made them better partners under drought, improving plant growth within just a few generations. Evolution occurred mainly on a specialized bacterial plasmid, a mobile piece of DNA distinct from the main genome. By contrast, added nitrogen fertilizer led to decreases in bacterial benefits. These findings suggest that mutualisms are not simply fragile in the face of global change, but can expand mutualistic benefits to buffer partners against stress. CLASSIFICATIONBiological Sciences, Evolution

evolutionary biology↗

bioRxiv2026

Negative frequency-dependent selection maintains partner quality variation in a keystone nutritional mutualism

Mutualisms, interactions that benefit both partners, are critical for promoting biodiversity and ecosystem resiliency, yet are considered evolutionarily unstable and vulnerable to global change. Understanding how genetic variation in mutualisms is maintained is key to predicting their future persistence and explaining their long evolutionary history. While theory addresses factors maintaining variation in partner quality (the fitness benefits partners provide), few studies have experimentally tested these mechanisms. Here, we experimentally evolved multiple replicate populations of rhizobia, nitrogen-fixing mutualists of legumes, varying in partner quality under contrasting environments: nitrogen (N)-supplemented or N-free conditions, with or without host plants. After one year of rhizobial evolution, we quantified selection on partner quality across environments and evaluated resulting changes in mutualism traits and population-level genetic diversity. Strikingly, selection on partner quality was population-dependent: high-quality strains were favoured when initially rare but disfavoured when common, revealing negative-frequency dependent dynamics that can maintain variation. Although neither nitrogen-supplementation nor host presence directly imposed selection, both were critical for preserving genetic diversity in rhizobia populations - fuel for ongoing evolution. By demonstrating negative-frequency dependent selection in the legume-rhizobium mutualism, our study reveals a dynamic more akin to antagonistic interactions than traditionally assumed. This overlooked mechanism may be the key to explaining the ecological and evolutionary persistence of mutualisms under changing environments. Significance StatementMutualisms are central to biodiversity, yet their stability is puzzling because the mechanisms thought to stabilize them tend to eliminate the genetic variation needed for continued adaptation, even though partners in nature show striking variation in quality. In an experimental evolution study of a keystone plant-microbe mutualism (legume-rhizobium symbiosis), we found that negative frequency-dependent selection allows high- and low-quality symbionts to coexist: high-quality strains are favoured only when rare. Environmental factors such as nitrogen addition or host presence did not alter which partners were selected, but they helped maintain genetic diversity needed for future adaptation. Our findings reveal an overlooked mechanism that stabilizes mutualisms and explain how these interactions can remain resilient under changing environmental conditions.

evolutionary biology↗

bioRxiv2025

Elevated CO2 induces phyllosphere community changes in soybean

Plant-associated microbiomes play significant roles in determining their hosts responses to stress, which is increasingly common in a rapidly changing world. For example, foliar endophytes can increase tolerance to drought and decrease herbivory. Global atmospheric changes, such as increased atmospheric carbon dioxide concentration ([CO2]), have the potential to directly and indirectly alter microbiome community structure in ways that affect host plants underscoring our need to understand how microbial communities in planta will change under global change. Here, we used a metabarcoding approach to assess community composition and network structure of bacterial and fungal phyllosphere microbiomes within soybean (Glycine max) exposed to ambient and elevated [CO2] in the field. We found that fungal community composition differed between soybean grown in elevated and ambient [CO2], while bacterial communities did not. Additionally, co-occurrence networks for both fungi and bacteria in elevated [CO2] exhibited marked changes compared to the ambient networks including the composition of hub taxa. Overall, our findings suggest that anthropogenic change, such as elevated [CO2], can cause profound shifts in community assembly of microbes within their plant hosts. Our findings may aid those developing agro-ecological strategies using microbes to improve crop traits, which necessitates understanding the drivers of microbiome community structure. HighlightLeaf-associated microbes benefit plants, but how climate change affects these communities remains unclear. We found that elevated CO2 shifted fungal and bacterial community composition and network structure within soybean leaves.

ecology↗

bioRxiv2025

A continuum of ecology and evolution contributes to mutualism breakdown between legumes and rhizobia

Ecology and evolution jointly shape community responses to environmental perturbations, yet these processes are often examined separately, even in microorganisms where both occur over short time-scales. For example, during mutualism breakdown, shifts in diverse microbial communities might coincide with evolutionary changes in mutualistic traits within key symbionts. Here we study the legume-rhizobium mutualism after 33 years of nitrogen fertilization. Pairing a manipulative inoculation study with full-length 16S rRNA amplicon sequencing provides incomparable resolution across biological scales: whole bacterial community, genus Rhizobium, Rhizobium ASVs, and symbiosis plasmids. Clover host plant growth is first limited by symbiont availability; clovers preferred partner declines in N-addition soils, while a diverse, largely uncharacterized Rhizobium community increases. This ecological change is compounded by a concurrent evolutionary decline in the quality of the preferred symbiont through changing frequencies of symbiotic plasmids. These shifts make mutualists both rarer and inferior, reducing the benefits hosts receive from mutualism.

microbiology↗

bioRxiv2024

Plasmid transmission dynamics and evolution of partner quality in a natural population of Rhizobium leguminosarum

Many bacterial traits important to host-microbe symbiosis are determined by genes carried on extrachromosomal replicons such as plasmids, chromids, and integrative and conjugative elements. Multiple such replicons often coexist within a single cell and, due to horizontal mobility, have patterns of variation and evolutionary histories that are distinct from each other and from the bacterial chromosome. In nitrogen-fixing Rhizobium, genes carried on multiple plasmids make up almost 50% of the genome, are necessary for the formation of symbiosis, and underlie bacterial traits including host plant benefits. Thus the genomics and transmission of plasmids in Rhizobium underlie the ecology and evolution of this important model symbiont. Here we leverage a natural population of clover-associated Rhizobium in which partner quality has declined in response to long-term nitrogen fertilization. We use 62 novel, reference-quality genomes to characterize 257 replicons in the plasmidome and study their genomics and transmission patterns. We find that, of the four most frequent plasmid types, two (types II & III) have more stable size, larger core genomes, and track the chromosomal phylogeny (display more vertical transmission), while others (types I & IV - the symbiosis plasmid, or pSym) vary substantially in size, shared gene content, and have phylogenies consistent with frequent horizontal transmission. We also find differentiation in pSym subtypes driven by long-term nitrogen fertilization. Our results highlight the variation in plasmid transmission dynamics within a single symbiont and implicate plasmid horizontal transmission in the evolution of partner quality. IMPORTANCEUnderstanding how bacterial genes move through natural populations is critical for understanding how bacterial traits evolve. The nitrogen-fixing bacterium Rhizobium leguminosarum lives in symbiosis with plants and is a model for studying how gene transmission from one cell to another on mobile genetic elements called plasmids impacts the evolution of bacteria and plants. Here we characterize the genomes of a natural bacterial population, then use novel approaches to show that mechanisms of plasmid gene transmission varies across multiple plasmid types possessed by R. leguminosarum. We find that changes in plasmid genes are associated with the decline of symbiotic partner quality in strains isolated from environments undergoing long-term fertilization. Together, these results underscore the importance of plasmid evolution in shaping ecosystem processes like nitrogen cycling. Our study provides a framework for probing the plasmid dynamics within natural bacterial populations and how plasmid transmission affects genetic diversity and ecological interactions in bacteria.

genomics↗

bioRxiv2021

The complex genetics of symbiotic extended phenotypes across environments in a model mutualism

A goal of modern biology is to develop the genotype-phenotype (G[->]P) map, a predictive understanding of how genomic information generates trait variation that forms the basis of both natural and managed communities. As microbiome research advances, however, it has become clear that many of these traits are symbiotic extended phenotypes, being governed by genetic variation encoded not only by the hosts own genome, but also by the genomes of myriad cryptic symbionts. Building a reliable G[->]P map therefore requires accounting for the multitude of interacting genes and even genomes involved in symbiosis. Here we use naturally-occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti paired with two genotypes of the host Medicago truncatula in four genome-wide association studies to study the genomic architecture of a key symbiotic extended phenotype - partner quality, or the fitness benefit conferred to a host by a particular symbiont genotype, within and across environmental contexts and host genotypes. We define three novel categories of loci in rhizobium genomes that must be accounted for if we want to build a reliable G[->]P map of partner quality; namely, 1) loci whose identities depend on the environment, 2) those that depend on the host genotype with which rhizobia interact, and 3) universal loci that are likely important in all or most environments. IMPORTANCEGiven the rapid rise of research on how microbiomes can be harnessed to improve host health, understanding the contribution of microbial genetic variation to host phenotypic variation is pressing, and will better enable us to predict the evolution of (and select more precisely for) symbiotic extended phenotypes that impact host health. We uncover extensive context-dependency in both the identity and functions of symbiont loci that control host growth, which makes predicting the genes and pathways important for determining symbiotic outcomes under different conditions more challenging. Despite this context-dependency, we also resolve a core set of universal loci that are likely important in all or most environments, and thus, serve as excellent targets both for genetic engineering and future coevolutionary studies of symbiosis.

evolutionary biology↗

bioRxiv2021

Partners in space: Discordant population structure between legume hosts and rhizobium symbionts in their native range

Coevolution is predicted to depend on how the genetic diversity of interacting species is geographically structured. Plant-microbe symbioses such as the legume-rhizobium mutualism are ecologically and economically important, but distinct life history and dispersal mechanisms for these host and microbial partners, plus dynamic genome composition in bacteria, present challenges for understanding spatial genetic processes in these systems. Here we study the model rhizobium Ensifer meliloti using a hierarchically-structured sample of 191 strains from 21 sites in the native range and compare its population structure to that of its host plant Medicago truncatula. We find high local genomic variation and minimal isolation by distance across the rhizobium genome, particularly at the two symbiosis elements pSymA and pSymB, which have evolutionary histories and population structures that are similar to each other but distinct from both the chromosome and the host. While the chromosome displays weak isolation by distance, it is uncorrelated with hosts. Patterns of discordant population structure among elements with the bacterial genome has implications for bacterial adaptation to life in the soil versus symbiosis, while discordant population genetic structure of hosts and microbes might restrict local adaptation of species to each other and give rise to phenotypic mismatches in coevolutionary traits.

evolutionary biology↗

bioRxiv2021

Dichaete, a Sox2 homologue, prevents activation of cell death in multiple developmental contexts

Precisely regulated cell death plays a critical role in normal development and is controlled by the balance of pro-apoptotic and anti-apoptotic signals. In Drosophila, transcription of the clustered cell death activators grim and reaper is turned on in the developing nervous system to eliminate neural stem cells at the end of embryonic development. This transcription is activated by a pulse of the Hox gene abdominal-A. We show here that the Sox2 homologue Dichaete inhibits neural stem cell death when overexpressed, and loss of Dichaete promotes premature neural stem cell death. The anti-apoptotic activity of Dichaete opposes the pro-apoptotic factors abdominal-A, as well as the transcription factor grainyhead. The function of all three genes impinge on an enhancer that regulates the transcription of grim and reaper. Furthermore, we find that the balance between abdominal-A and Dichaete is likely to regulate the death of other cells during development, including cells in the developing midline, the developing hindgut, and in the early abdominal epidermis. Loss of Dichaete results in premature death in these tissues. This death can be rescued by the deletion of the enhancer region between grim and reaper. These data suggest that Dichaete functions to inhibit cell death activated by abdominal-A in multiple developmental contexts.

developmental biology↗

bioRxiv2019

Comprehensive characterization of the mutational landscape in localized anal squamous cell carcinoma

PurposeAnal squamous cell carcinoma (ASCC) is a rare neoplasm. Chemo-radiotherapy is the standard of care, with no therapeutic advances achieved over the past three decades. Thus, a deeper molecular characterization of this disease is still necessary.\n\nMethodsWe analyzed 46 paraffin-embedded tumor samples from patients diagnosed with primary ASCC by exome sequencing. A bioinformatics approach focused in the identification of high impact genetic variants, which may act as drivers of oncogenesis, was performed. The relation between genetics variant and prognosis was also studied.\n\nResultsThe list of high impact genetic variants was unique for each patient. However, the pathways in which these genes are involved are well-known hallmarks of cancer, such as angiogenesis or immune pathways. Additionally, we determined that genetic variants in BRCA2, ZNF750, FAM208B, ZNF599 and ZC3H13 genes are related with poor disease-free survival in ASCC.\n\nConclusionHigh impact genetic variants in ASCC affect pathways involved in cancer development, and may play a role in the etiology of the disease. Variants in BRCA2, ZNF750, FAM208B, ZNF599 and ZC3H13 genes seem to be related with prognosis in ASCC. Sequencing of ASCC clinical samples appears an encouraging tool for the molecular portrait of this disease.

cancer biology↗

bioRxiv2018

Differential effects of conspecific and heterospecific density on the development of Aedes aegypti and Aedes albopictus larvae

O_LIBetween-species competition shapes the distribution and abundance of populations. Aedes aegypti and Ae. albopictus are vectors of pathogens such as dengue and are known to compete at the larval stage.\nC_LIO_LIThe outcome of this inter-species competition has been found to be context dependent, with the strength and direction changing with resource availability and type. We were motivated by this uncertainty, and aimed to elucidate the magnitude and mechanism of competition.\nC_LIO_LIWe manipulated the larval density of mixed and single species cohorts of larvae, measuring the effects on survivorship and development time. Unlike other related studies, we adjusted the feeding regime so that the per-capita resource availability was kept constant across all density treatments, at a level sufficient for successful development. This ensured that each larvae at least had the opportunity to gain the requisite resources for pupation.\nC_LIO_LIOur analysis found that Ae. aegypti suffered notably less mortality due to intra- and interspecific competition. For both species, intra- and interspecific competition led to the survival of faster developing individuals, with the exception that slower developing Ae. albopictus larvae survived when exposed a combination of both high con- and heterospecific densities.\nC_LIO_LIThese results show that the competition between Ae. aegypti and Ae. albopictus can still occur even when resources are theoretically adequate for development. This suggests that larvae can alter resource seeking and consumption parameters when exposed to high densities of conspecifics and heterospecifics, leading to contest competition. Evidence for resource-independent mechanisms of competition such as crowding are also found, as is evidence for the importance of demographic stochasticity in population processes.\nC_LI

ecology↗

bioRxiv2017

xenoGI: reconstructing the history of genomic island insertions in clades of closely related bacteria

BackgroundGenomic islands play an important role in microbial genome evolution, providing a mechanism for strains to adapt to new ecological conditions. A variety of computational methods, both genome-composition based and comparative have been developed to identify them. Some of these methods are explicitly designed to work in single strains, while others make use of multiple strains. In general, existing methods do not identify islands in the context of the phylogeny in which they evolved. Even multiple strain approaches are best suited to identifying genomic islands that are present in one strain but absent in others. They do not automatically recognize islands which are shared between some strains in the clade or determine the branch on which these islands inserted within the phylogenetic tree.\n\nResultsWe have developed a software package, xenoGI, that identifies genomic islands and maps their origin within a clade of closely related bacteria, determining which branch they inserted on. It takes as input a set of sequenced genomes and a tree specifying their phylogenetic relationships. Making heavy use of synteny information, the package builds gene families in a species-tree-aware way, and then attempts to combine into islands those families whose members are adjacent and whose most recent common ancestor is shared. The package provides a variety of text-based analysis functions, as well as the ability to export genomic islands into formats suitable for viewing in a genome browser. We demonstrate the capabilities of the package with several examples from enteric bacteria, including an examination of the evolution of the acid fitness island in the genus Escherichia. In addition we use output from simulations and a set of known genomic islands from the literature to show that xenoGI can accurately identify genomic islands and place them on a phylogenetic tree.\n\nConclusionsxenoGI is an effective tool for studying the history of genomic island insertions in a clade of microbes. It identifies genomic islands, and determines which branch they inserted on within the phylogenetic tree for the clade. Such information is valuable because it helps us understand the adaptive path that has produced living species. Given the large and growing number of sequenced microbial genomes, this sort of analysis will become increasingly useful in the future.

bioinformatics↗

bioRxiv2017

Geographically structured genetic variation in the Medicago lupulina-Ensifer mutualism

Mutualisms are interspecific interactions affecting the ecology and evolution of species. Patterns of geographic variation in interacting species may play an important role in understanding how variation is maintained in mutualisms, particularly in introduced ranges. One agriculturally and ecologically important mutualism is the partnership between legume plants and rhizobia. Through characterizing and comparing the population genomic structure of the legume Medicago lupulina and two rhizobial species (Ensifer medicae and E. meliloti), we explored the spatial scale of population differentiation between interacting partners in their introduced range in North America. We found high proportions of E. meliloti in southeastern populations and high proportions of E. medicae in northwestern populations. Medicago lupulina and the Ensifer genus showed similar patterns of spatial genetic structure (isolation by distance). However, we detected no evidence of isolation by distance or population structure within either species of bacteria. Genome-wide nucleotide diversity within each of the two Ensifer species was low, suggesting limited introduction of strains, founder events, or severe bottlenecks. Our results suggest that there is potential for geographically structured coevolution between M. lupulina and the Ensifer genus, but not between M. lupulina and either Ensifer species.

evolutionary biology↗