More Like this

1. Pangenome Evolution Reconciles Robustness and Instability of Rhizobial Symbiosis

   https://doi.org/10.1128/mbio.00074-22  

   Weisberg, Alexandra J.; Rahman, Arafat; Backus, Dakota; Tyavanagimatt, Parinita; Chang, Jeff H.; Sachs, Joel L. (June 2022, mBio)

   Cooper, Vaughn S. (Ed.)

   ABSTRACT Root nodulating rhizobia are nearly ubiquitous in soils and provide the critical service of nitrogen fixation to thousands of legume species, including staple crops. However, the magnitude of fixed nitrogen provided to hosts varies markedly among rhizobia strains, despite host legumes having mechanisms to selectively reward beneficial strains and to punish ones that do not fix sufficient nitrogen. Variation in the services of microbial mutualists is considered paradoxical given host mechanisms to select beneficial genotypes. Moreover, the recurrent evolution of non-fixing symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. Here, we deconstructed hundreds of genome sequences from genotypically and phenotypically diverse Bradyrhizobium strains and revealed mechanisms that generate variation in symbiotic nitrogen fixation. We show that this trait is conferred by a modular system consisting of many extremely large integrative conjugative elements and few conjugative plasmids. Their transmissibility and propensity to reshuffle genes generate new combinations that lead to uncooperative genotypes and make individual partnerships unstable. We also demonstrate that these same properties extend beneficial associations to diverse host species and transfer symbiotic capacity among diverse strains. Hence, symbiotic nitrogen fixation is underpinned by modularity, which engenders flexibility, a feature that reconciles evolutionary robustness and instability. These results provide new insights into mechanisms driving the evolution of mobile genetic elements. Moreover, they yield a new predictive model on the evolution of rhizobial symbioses, one that informs on the health of organisms and ecosystems that are hosts to symbionts and that helps resolve the long-standing paradox. IMPORTANCE Genetic variation is fundamental to evolution yet is paradoxical in symbiosis. Symbionts exhibit extensive variation in the magnitude of services they provide despite hosts having mechanisms to select and increase the abundance of beneficial genotypes. Additionally, evolution of uncooperative symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. We analyzed genome sequences of Bradyrhizobium, bacteria that in symbioses with legume hosts, fix nitrogen, a nutrient essential for ecosystems. We show that genes for symbiotic nitrogen fixation are within elements that can move between bacteria and reshuffle gene combinations that change host range and quality of symbiosis services. Consequently, nitrogen fixation is evolutionarily unstable for individual partnerships, but is evolutionarily stable for legume- Bradyrhizobium symbioses in general. We developed a holistic model of symbiosis evolution that reconciles robustness and instability of symbiosis and informs on applications of rhizobia in agricultural settings. 

   more » « less
2. Recurrent mutualism breakdown events in a legume rhizobia metapopulation

   https://doi.org/10.1098/rspb.2019.2549  

   Gano-Cohen, Kelsey A.; Wendlandt, Camille E.; Al Moussawi, Khadija; Stokes, Peter J.; Quides, Kenjiro W.; Weisberg, Alexandra J.; Chang, Jeff. H.; Sachs, Joel L. (January 2020, Proceedings of the Royal Society B: Biological Sciences)

   Bacterial mutualists generate major fitness benefits for eukaryotes, reshaping the host phenotype and its interactions with the environment. Yet, microbial mutualist populations are predicted to generate mutants that defect from providing costly services to hosts while maintaining the capacity to exploit host resources. Here, we examined the mutualist service of symbiotic nitrogen fixation in a metapopulation of root-nodulating Bradyrhizobium spp . that associate with the native legume Acmispon strigosus . We quantified mutualism traits of 85 Bradyrhizobium isolates gathered from a 700 km transect in California spanning 10 sampled A. strigosus populations. We clonally inoculated each Bradyrhizobium isolate onto A. strigosus hosts and quantified nodulation capacity and net effects of infection, including host growth and isotopic nitrogen concentration. Six Bradyrhizobium isolates from five populations were categorized as ineffective because they formed nodules but did not enhance host growth via nitrogen fixation. Six additional isolates from three populations failed to form root nodules. Phylogenetic reconstruction inferred two types of mutualism breakdown, including three to four independent losses of effectiveness and five losses of nodulation capacity on A. strigosus . The evolutionary and genomic drivers of these mutualism breakdown events remain poorly understood. 

   more » « less
3. Light availability and rhizobium variation interactively mediate the outcomes of legume–rhizobium symbiosis

   https://doi.org/10.1002/ajb2.1435  

   Heath, Katy_D; Podowski, Justin_C; Heniff, Stephanie; Klinger, Christie_R; Burke, Patricia_V; Weese, Dylan_J; Yang, Wendy_H; Lau, Jennifer_A (February 2020, American Journal of Botany)

   PremiseNutrients, light, water, and temperature are key factors limiting the growth of individual plants in nature. Mutualistic interactions between plants and microbes often mediate resource limitation for both partners. In the mutualism between legumes and rhizobia, plants provide rhizobia with carbon in exchange for fixed nitrogen. Because partner quality in mutualisms is genotype‐dependent, within‐species genetic variation is expected to alter the responses of mutualists to changes in the resource environment. Here we ask whether partner quality variation in rhizobia mediates the response of host plants to changing light availability, and conversely, whether light alters the expression of partner quality variation. MethodsWe inoculated clover hosts with 11 strains ofRhizobium leguminosarumthat differed in partner quality, grew plants under either ambient or low light conditions in the greenhouse, and measured plant growth, nodule traits, and foliar nutrient composition. ResultsLight availability and rhizobium inoculum interactively determined plant growth, and variation in rhizobium partner quality was more apparent in ambient light. ConclusionsOur results suggest that variation in the costs and benefits of rhizobium symbionts mediate host responses to light availability and that rhizobium strain variation might more important in higher‐light environments. Our work adds to a growing appreciation for the role of microbial intraspecific and interspecific diversity in mediating extended phenotypes in their hosts and suggests an important role for light availability in the ecology and evolution of legume–rhizobium symbiosis. 

   more » « less
4. Experimental evolution can enhance benefits of rhizobia to novel legume hosts

   https://doi.org/10.1098/rspb.2021.0812  

   Quides, Kenjiro W.; Weisberg, Alexandra J.; Trinh, Jerry; Salaheldine, Fathi; Cardenas, Paola; Lee, Hsu-Han; Jariwala, Ruchi; Chang, Jeff H.; Sachs, Joel L. (May 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Legumes preferentially associate with and reward beneficial rhizobia in root nodules, but the processes by which rhizobia evolve to provide benefits to novel hosts remain poorly understood. Using cycles of in planta and in vitro evolution, we experimentally simulated lifestyles where rhizobia repeatedly interact with novel plant genotypes with which they initially provide negligible benefits. Using a full-factorial replicated design, we independently evolved two rhizobia strains in associations with each of two Lotus japonicus genotypes that vary in regulation of nodule formation. We evaluated phenotypic evolution of rhizobia by quantifying fitness, growth effects and histological features on hosts, and molecular evolution via genome resequencing. Rhizobia evolved enhanced host benefits and caused changes in nodule development in one of the four host–symbiont combinations, that appeared to be driven by reduced costs during symbiosis, rather than increased nitrogen fixation. Descendant populations included genetic changes that could alter rhizobial infection or proliferation in host tissues, but lack of evidence for fixation of these mutations weakens the results. Evolution of enhanced rhizobial benefits occurred only in a subset of experiments, suggesting a role for host–symbiont genotype interactions in mediating the evolution of enhanced benefits from symbionts. 

   more » « less
5. Genetic variation in Breviolum antillogorgium , a coral reef symbiont, in response to temperature and nutrients

   https://doi.org/10.1002/ece3.4959  

   Bayliss, Shannon L.; Scott, Zoë R.; Coffroth, Mary Alice; terHorst, Casey P. (February 2019, Ecology and Evolution)

   Abstract Symbionts within the familySymbiodiniaceaeare important on coral reefs because they provide significant amounts of carbon to many different reef species. The breakdown of this mutualism that occurs as a result of increasingly warmer ocean temperatures is a major threat to coral reef ecosystems globally. Recombination during sexual reproduction and high rates of somatic mutation can lead to increased genetic variation within symbiont species, which may provide the fuel for natural selection and adaptation. However, few studies have asked whether such variation in functional traits exists within these symbionts. We used several genotypes of two closely related species,Breviolum antillogorgiumandB. minutum, to examine variation of traits related to symbiosis in response to increases in temperature or nitrogen availability in laboratory cultures. We found significant genetic variation within and among symbiont species in chlorophyll content, photosynthetic efficiency, and growth rate. Two genotypes showed decreases in traits in response to increased temperatures predicted by climate change, but one genotype responded positively. Similarly, some genotypes within a species responded positively to high‐nitrogen environments, such as those expected within hosts or eutrophication associated with global change, while other genotypes in the same species responded negatively, suggesting context‐dependency in the strength of mutualism. Such variation in traits implies that there is potential for natural selection on symbionts in response to temperature and nutrients, which could confer an adaptive advantage to the holobiont. 

   more » « less