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Lau, J. A.

Publications and source records attributed to Lau, J. A..

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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↗

Microbe-mediated plant acclimation to drought may be rare in agriculture

Microbial communities can shift under drought in ways that enhance plant performance during drought ("microbe-mediated acclimation"). However, it is also possible for microbial communities to shift in ways that worsen the effects of drought ("mal-acclimation"). It is unclear how and where microbe-mediated acclimation vs. mal-acclimation occurs, or if there are types of soils or microbial communities that are more likely to harbor microbes that enhance plant acclimation and limit mal-acclimation. We tested for microbe-mediated plant acclimation/mal-acclimation to drought in soils from 21 maize farms in the midwestern United States, spanning a range of climate, soil types, and management practices. We first conditioned soil microbial communities to drought vs. well-watered conditions in a greenhouse and then tested for microbe-mediated acclimation by growing maize in soils inoculated with the conditioned microbial communities under drought and well-watered conditions. Drought-conditioned soils did not enhance plant performance under drought. In fact, one third of the farms exhibited mal-acclimation, especially under well-watered conditions where wet-conditioned soils reduced plant performance in well-watered contemporary conditions. Farm management practices, climate, soil texture, and microbial diversity generally did not predict when this microbe-mediated mal-acclimation occurred. Overall, these results suggest that in agricultural soils, microbes may frequently impede-rather than facilitate-plant acclimation to soil moisture levels. Open research statementThe plant and soil data used in this study are available via the Environmental Data Initiative repository at https://doi.org/10.6073/pasta/f4a0db3a076cf6d8cef908947f82736e. The bacterial and fungal amplicon sequence data are available via the European Nucleotide Archive under accessions PRJEB110071 and PRJEB109827, respectively.

ecology↗

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↗

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↗

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↗

Microbial responses to stress cryptically alter natural selection on plants

O_LIMicrobial communities can rapidly respond to stress, meaning plants may encounter altered soil microbial communities in stressful environments. These altered microbial communities may then affect natural selection on plants. Because stress can cause lasting changes to microbial communities, microbes may also cause legacy effects on plant selection that persist even after the stress ceases. C_LIO_LITo explore how microbial responses to stress and persistent microbial legacy effects of stress affect natural selection, we grew Chamaecrista fasciculata plants in stressful (salt, herbicide, or herbivory) or non-stressful conditions with microbes that had experienced each of these environments in the previous generation. C_LIO_LIMicrobial community responses to stress generally counteracted the effects of stress itself on plant selection, thereby weakening the strength of stress as a selective agent. Microbial legacy effects of stress altered plant selection in non-stressful environments, suggesting that stress-induced changes to microbes may continue to affect selection after stress is lifted. C_LIO_LIThese results suggest that soil microbes may play a cryptic role in plant adaptation to stress, potentially reducing the strength of stress as a selective agent and altering the evolutionary trajectory of plant populations. C_LI

ecology↗

Traits of soil bacteria predict plant responses to soil moisture

Microbes can promote beneficial plant and animal responses to abiotic environments, but the ecological drivers of this benefit remain elusive. Here we investigated byproduct benefits, which occur when traits that increase the fitness of one species provide incidental benefits to another species with no direct cost to the provider species. In experimental mesocosms, microbial traits predicted plant responses to soil moisture such that bacteria with self-beneficial traits in drought increased plant early growth, size at reproduction, and chlorophyll concentration under drought, while bacteria with self-beneficial traits in well-watered environments increased these same plant traits in well-watered environments. Thus, microbial traits that promote microbial success in different soil moisture environments also promote plant success in these same environments. Our results show that the concept of byproduct benefits, originally conceived to explain the evolution of cooperation in pairwise mutualisms, also applies to interactions between plants and non-symbiotic soil microbes.

ecology↗

Evolution in novel environments: do restored prairie populations experience strong selection?

When populations colonize new habitats, they are likely to experience novel environmental conditions, and as a consequence may experience strong selection. While selection and the resulting evolutionary responses may have important implications for establishment success in colonizing populations, few studies have estimated selection in such scenarios. Here we examined evidence of selection in recently established plant populations in two prairie restorations in close proximity (< 15 km apart) using two approaches: 1) we tested for evidence of past selection on a suite of traits in two Chamaecrista fasciculata populations by comparing the restored populations to each other and their shared source population in common gardens to quantify evolutionary responses and 2) we measured selection in the field. We found evidence of past selection on flowering time, specific leaf area, and root nodule production in one of the populations, but detected contemporary selection on only one trait (plant height). This demonstrates that while selection can occur in colonizing populations, resulting in significant evolutionary responses in less than 6 generations, rapid evolutionary responses may be weak in even nearby populations sown with the same source population. Because contemporary measures of selection rarely predicted observed evolutionary responses, it also suggests that selection likely differs over the early stages of succession that characterize young prairies.

evolutionary biology↗