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Ravenscraft, A.

Publications and source records attributed to Ravenscraft, A..

6 recordsLinked to original sources

Microbial Thermal Response Strategies Impact Environmental Fitness of Horizontally Transmitted Symbiont Strains

Microbial symbionts in insect-microbe mutualisms are critical for host survival and fitness. However, symbioses are sensitive to external stressors. Understanding how a warming climate will impact these associations, therefore, is critical. Previous work on horizontally transmitted bug-Caballeronia bacterial symbionts has shown that different symbiont strains confer variable host outcomes under thermal stress, suggesting that environmental symbiont acquisition could be advantageous under shifting temperature regimes. However, it is unknown what specific bacterial thermal responses could impact microbial survival in the environment, which would be key to host acquisition. We evaluated in vitro thermal response mechanisms of heat-vulnerable and heat-resistant strains of Caballeronia using microbial transcripts, to identify pathways that may impact the symbionts respective thermal optima. We found that a heat-resistant strain prioritizes induction of thermally stable outer membrane components, motility structures, and molecular chaperones, allowing it to increase growth through induction of central metabolism and protein synthesis. Meanwhile, a heat-vulnerable strain arrests growth, favoring induction of genes related to alternative metabolism and biofilm formation. These results are indicative of variable bacterial thermal response strategies for elevated temperature survival. Ultimately these responses may alter which symbionts are more available to insect hosts as temperatures continue to rise. ImportanceMany eukaryotes host beneficial microbes that synthesize essential nutrients or can break down harmful compounds. While important, if these microbes are acquired from the local environment (i.e., soils or plant surfaces), external stressors can destabilize the associations by impacting microbial growth, limiting the pool of available microbes. Using the bug-Caballeronia model system, we analyzed the in vitro thermal stress response of two Caballeronia symbiont strains that have different thermal optima. We found that stress responses involving increased motility, thermally stable membrane synthesis, and molecular chaperones may increase growth under thermal stress in symbionts. These results indicate that different thermal stress coping strategies may be favored in bug-Caballeronia system under increasing global temperatures. More broadly, these results provide insight into how microbial stress responses could shape adaptation of symbioses to a warming climate.

bioinformatics↗

Leaffooted bugs enrich local soil with their horizontally acquired symbiont

Associations between hosts and their microbial symbionts are considered mutualistic when both partners benefit. While the advantages received by eukaryotic hosts from association with bacterial symbionts are frequently examined, benefits to the bacteria are rarely experimentally tested. Here, we consider whether the bug-Caballeronia symbiosis is truly mutualistic by measuring the effect of a leaffooted bug (Leptoglossus phyllopus) on the abundance of its horizontally acquired symbiont, Caballeronia grimmiae. We predicted that the free-living Caballeronia population would increase over time in the presence of its insect partner. We quantified Caballeronia titer in soil microcosms (i) in the presence and absence of L. phyllopus over time, and (ii) at different bug densities. Insect presence resulted in higher soil Caballeronia titer over time. As bug density increased, the soil Caballeronia population also increased. Additionally, soil moisture affected Caballeronia abundance, with moister soil supporting a larger population. These results demonstrate that the relationship between Caballeronia and L. phyllopus is truly mutualistic and add to a small but growing body of literature that has quantified the effects of eukaryotic hosts on their bacterial partners.

microbiology↗

Species-specific bacterial associations emerge from stochastically assembled microbiomes in Northeastern American fireflies

Many insects harbor diverse microbial communities ("microbiomes") that can profoundly influence the biology of their host. Yet, for most insect taxa, the relative roles of stochastic events versus deterministic forces in shaping these communities remain unknown. We investigated microbiome assembly in fireflies (Coleoptera: Lampyridae) using 16S rRNA gene amplicon sequencing and quantitative PCR from 12 species and species groups collected across the Northeastern United States. We hypothesized that firefly microbiomes are predominantly structured by stochastic ecological processes, such as random microbial exposures. Consistent with this, we observed elevated normalized stochasticity ratio (NST) values for most bacteria, coupled with high intraspecific variability in bacterial abundance and composition. However, microbiomes were more similar among closely related firefly hosts, and several bacterial taxa, including endosymbionts and unusually prevalent mollicute strains, showed lower NST values, species-specific associations, and patterns linked to geography, season, and sex. These results reveal that deterministic processes--likely involving host-driven microbial filtering, microbe-microbe interactions, and reliable transmission modes--act alongside stochastic forces to shape firefly-microbe associations. By disentangling these ecological drivers in a diverse, understudied beetle lineage, our study advances understanding of the ecological and evolutionary processes structuring microbiomes in the wild.

ecology↗

Enantiomer-Specific Malathion Degradation by Gut Microbes of the Colorado Potato Beetle

Symbiotic microbes play pivotal roles in insect ecology, including the detoxification of insecticides, which reduces target host mortality and diminishes the efficacy of chemical pest control agents. Quantifying the prevalence of symbiont-mediated insecticide detoxification across the microbiome is necessary to understand its contributions to pesticide resistance, and to understand how pesticides alter gut microbial communities. Here, we investigated the prevalence and mechanisms of pesticide degradation within the gut microbiota of the Colorado potato beetle (Leptinotarsa decemlineata), a significant agricultural pest that has driven ongoing insecticide innovation for decades. Beetles were collected from an organic farm in Tyler, TX, and 18 bacterial isolates representing the diversity of their gut microbiota were screened for their ability to degrade three common insecticides in vitro: imidacloprid, fenitrothion, and malathion. Among these, Acinetobacter calcoaceticus, Pseudomonas protegens, and an unnamed Microbacterium species degraded malathion as a sole carbon source, with distinct enantiomer-specific preferences. Untargeted GC-MS analysis revealed breakdown products, providing initial insights into the metabolic pathways utilized by these microbes. These findings suggest that microbial association with resistant insect hosts may select for microbial insecticide utilization, potentially enhancing resistance development in agricultural pests and influencing the surrounding soil microbiome.

microbiology↗

The facultative intracellular symbiont Lariskella is neutral for lifetime fitness and spreads through cytoplasmic incompatibility in the leaffooted bug, Leptoglossus zonatus

The maternally-inherited, intracellular bacterium Lariskella (Alphaproteobacteria: Midichloreaceae) has been widely detected in arthropods including true bugs, beetles, a wasp, a moth, and pathogen-vectoring fleas and ticks. Despite its prevalence, its role in the biology of its hosts has been unknown. We set out to determine the role of this symbiont in the leaffooted bug, Leptoglossus zonatus (Hempitera: Coreidae). To examine the effects of Lariskella on bug performance and reproduction as well as in possible interactions with the bugs obligate nutritional symbiont, Caballeronia, bugs were reared in a factorial experiment with both Lariskella and Caballeronia positive and negative treatments. Lifetime survival analysis ([~]120 days) showed significant developmental delays and decrease in survival for bugs that lacked Caballeronia, and Caballeronia-free bugs did not reproduce. However, among the Caballeronia carrying treatments, there were no significant differences in lifetime survival or reproduction in treatments with and without Lariskella, suggesting this symbiont is neutral for overall bug fitness. To test for reproductive manipulation, crossing among Lariskella-positive and negative individuals was performed. When Lariskella-negative females were mated with Lariskella positive males, fewer eggs survived early embryogenesis, consistent with a cytoplasmic incompatibility (CI) phenotype. Wild L. zonatus from California and Arizona showed high but not fixed Lariskella infection rates. Within individuals, Lariskella titer was low during early development (1st-3rd instar), followed by an increase that coincided with development of reproductive tissues. Our results reveal Lariskella to be among a growing number of microbial symbionts that cause CI, a phenotype that increases the relative fitness of females harboring the symbiont. Understanding the mechanism of how Lariskella manipulates reproduction can provide insights into the evolution of reproductive manipulators and may eventually provide tools for management of hosts of Lariskella, including pathogen-vectoring ticks and fleas. Author SummaryArthropods are a highly diverse group of animals with ancient relationships with bacteria. Some maternally-inherited, intracellular bacterial symbionts have evolved strategies to manipulate arthropod host reproduction, ensuring their own spread and persistence. One such strategy is cytoplasmic incompatibility (CI), where symbionts in males prevent viable offspring when these males mate with uninfected females. However, reproduction is rescued in crosses with both mates infected, promoting bacterial transmission within host populations. In the leaffooted bug Leptoglossus zonatus, crossing experiments revealed a significant reduction in egg survival rates when Lariskella-negative females mated with Lariskella-positive males, a typical CI phenotype discovered anew for this symbiont. Additional experiments included measuring performance and fitness of bugs with combinations of Lariskella and Caballeronia (the primary nutritional symbiont of L. zonatus). While Caballeronia-negative treatments caused developmental delays and mortality, the presence of Lariskella had no effect on development or reproduction. Lariskella has been frequently found in pathogen-vectoring arthropods, but its specific role remained unclear. Understanding the role that Lariskella plays in L. zonatus can potentially help us find future pest control measures against blood-sucking pathogen-vectors by exploiting novel CI mechanism to suppress host populations and hence the transmission of human diseases.

ecology↗

Structure and function of the bacterial and fungal gut flora of Neotropical butterflies

The relationship between animals and their gut flora is simultaneously one of the most common and most complex symbioses on Earth. Despite its ubiquity, our understanding of this invisible but often critical relationship is still in its infancy. We employed adult Neotropical butterflies as a study system to ask three questions: First, how does gut microbial community composition vary across host individuals, species and dietary guilds? Second, how do gut flora compare to food microbial communities? Finally, are gut flora functionally adapted to the chemical makeup of host foods? To answer these questions we captured nearly 300 Costa Rican butterflies representing over 50 species, six families and two feeding guilds: frugivores and nectivores. We characterized the bacteria and fungi in guts, wild fruits and wild nectars via amplicon sequencing and assessed the catabolic abilities of the gut flora via culture-based assays.\n\nGut communities were distinct from food communities, suggesting that the gut environment acts as a strong filter on potential colonists. Nevertheless, gut flora varied widely among individuals and species. On average, a pair of butterflies shared 21% of their bacterial species and 6% of their fungi. Host species explained 25-30% of total variation in microbial communities while host diet explained 4%. However, diet was still relevant at the individual microbe level--half of the most abundant microbial species differed in abundance between frugivores and nectivores. Diet was also related to the functional profile of gut flora: compared to frugivores, nectivores gut flora exhibited increased catabolism of sugars and sugar alcohols and decreased catabolism of amino acids, carboxylic acids and dicarboxylic acids. Since fermented juice contains more amino acids and less sugar than nectar, it appears that host diet filters the gut flora by favoring microbes that digest compounds abundant in foods.\n\nBy quantifying the degree to which gut communities vary among host individuals, species and dietary guilds and evaluating how gut microbial composition and catabolic potential are related to host diet, this study deepens our understanding of the structure and function of one of the most complex and ubiquitous symbioses in the animal kingdom.

ecology↗