Biology subjects

Goldstein, E. B.

Publications and source records attributed to Goldstein, E. B..

4 recordsLinked to original sources

bioRxiv2025

Phenotypic divergence is driven by mobile genetic elements in a heritable insect symbiont

AO_SCPLOWBSTRACTC_SCPLOWHeritable microbes profoundly influence insect biology, yet the traits they confer often evolve rapidly and differ among closely related symbiont strains. Despite their importance, we lack a clear understanding of how novel traits arise in symbiosis and how this diversity influences host ecology in natural populations. The aphid facultative symbiont Regiella insecticola is ideally suited to this question because of its strong lineage-specific variation in host benefits. By generating 20 high-quality genomes, we found that Regiellas evolution is driven largely by gene gains mediated by mobile genetic elements. We identified a plasmid (pRILSR1) that encodes a type IV secretion system and a highly expressed predicted effector that has been convergently acquired by Regiella strains from pea aphids. Notably, only pRILSR1-bearing strains confer protection against the specialist fungal pathogen Pandora neoaphidis, indicating that gains and losses of the plasmid underlie the evolution of this key defensive phenotype. Using a multi-year field study, we further show that the pRILSR1 plasmid is strongly associated with Regiella found in pea aphid populations adapted to specific host plants, driving variation in symbiont-mediated defense across populations. Together, our results show that mobile genetic elements generate key adaptive traits in microbial symbionts and, in doing so, drive phenotypic divergence among host populations.

evolutionary biology↗

bioRxiv2023

Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

AO_SCPLOWBSTRACTC_SCPLOWBacteria shape interactions between hosts and fungal pathogens. In some cases, bacteria associated with fungi are essential for pathogen virulence. In other systems, host associated microbiomes confer resistance against fungal pathogens. We studied an aphid-specific entomopathogenic fungus called Pandora neoaphidis in the context of both host and pathogen microbiomes. Aphids host several species of heritable bacteria, some of which confer resistance against Pandora. We first found that spores that emerged from aphids that harbored protective bacteria were less virulent against subsequent hosts and did not grow on plate media. We then used 16S amplicon sequencing to study the bacterial microbiome of fungal mycelia and spores during plate culturing and host infection. We found that the bacterial community is remarkably stable in culture despite dramatic changes in pathogen virulence. Last, we used an experimentally transformed symbiont of aphids to show that Pandora can acquire hostassociated bacteria during infection. Our results uncover new roles for bacteria in the dynamics of aphidpathogen interactions and illustrate the importance of the broader microbiological context in studies of fungal pathogenesis.

microbiology↗

bioRxiv2022

Variation in density, immune gene suppression, and co-infection outcomes among strains of the aphid endosymbiont Regiella insecticola

AO_SCPLOWBSTRACTC_SCPLOWMany insects harbor heritable beneficial microbes that influence host phenotypes. Across systems, divergent symbiont strains have been shown to establish at different densities within hosts. This genetic variation is important evolutionarily because within-host density has been linked to the costs and benefits of the symbiosis for both partners. Studying the factors shaping within-host density is therefore important to our broader understanding of host-microbe coevolution. Here we focused on different strains of Regiella insecticola, a facultative symbiont of aphids. We first demonstrated that different strains of Regiella consistently establish in pea aphids at drastically different densities. We then found that variation in density is correlated with the expression levels of two key insect immune system genes (phenoloxidase and hemocytin), with immune gene suppression correlating with higher Regiella density. We then performed an experiment where we established co-infections of a higher- and lower-density Regiella strain, and we showed that the higher-density strain is better able to persist in co-infections than the lower-density strain. Together, our results point to a potential mechanism for strain-level variation in symbiont density in this system, and further suggest that symbiont fitness may be increased by establishing at higher density within hosts. Our work highlights the importance of within-host dynamics shaping symbiont evolution.

evolutionary biology↗

bioRxiv2020

Intraspecific variation in immune gene expression and heritable symbiont density

AO_SCPLOWBSTRACTC_SCPLOWHost genetic variation plays an important role in the structure and function of heritable microbial communities. Recent studies have demonstrated that insects use immune mechanisms to regulate heritable symbionts. Here we test the hypothesis that variation in symbiont density within hosts is linked to intraspecific differences in the immune response to harboring symbionts. We show that pea aphids (Acyrthosiphon pisum) harboring the bacterial endosymbiont Regiella insecticola (but not all other species of symbionts) suppress expression of key immune genes. We then functionally link immune suppression with symbiont density using RNAi. The pea aphid species complex is comprised of multiple reproductively-isolated host plant-adapted populations. These biotypes have distinct patterns of heritable symbiont infections: for example, aphids from the Trifolium biotype are strongly associated with Regiella. Using RNAseq, we compare patterns of gene expression in response to Regiella in aphid genotypes from multiple biotypes, and we show that Trifolium aphids experience no immune gene suppression from Regiella and host symbionts at lower densities. We then generated F1 hybrids between two biotypes and found that symbiont density and immune suppression are both intermediate in hybrids. We suggest that in this system, Regiella symbionts are suppressing aphid immune mechanisms to increase their density, but that some hosts have adapted to prevent immune suppression in order to control symbiont numbers. The specific immune mechanisms suppressed by Regiella have been previously demonstrated to combat pathogens in aphids, and thus this work highlights the immune systems complex dual role in interacting with both beneficial and harmful microbes. AO_SCPLOWUTHORC_SCPLOW SO_SCPLOWUMMARYC_SCPLOWHeritable microbes are found in most insects including agriculturally and medically relevant pests. Explaining the variation in the distribution and abundance of symbionts in natural populations is critical to understanding these interactions. This work contributes to our mechanistic understanding of an important model of host-microbe symbiosis and suggests more broadly that variation in insect immune responses plays a role in intraspecific variation in host-symbiont interactions. Our work also suggests that antagonistic coevolution can play a role in host-microbe interactions even when microbes are transmitted vertically and provide a clear benefit to their hosts.

evolutionary biology↗