Biology subjects

Palmer-Young, E. C.

Publications and source records attributed to Palmer-Young, E. C..

9 recordsLinked to original sources

bioRxiv2024

Somy evolution in the honey bee infecting trypanosomatid parasite, Lotmaria passim

Lotmaria passim is a ubiquitous trypanosomatid parasite of honey bees nestled within the medically important subfamily Leishmaniinae. Although this parasite is associated with honey bee colony losses, the original draft genome--which was completed before its differentiation from the closely related Crithidia mellificae--has remained the reference for this species despite lacking improvements from newer methodologies. Here we report the updated sequencing, assembly, and annotation of the BRL type strain (ATCC PRA-422) of Lotmaria passim. The nuclear genome assembly has been resolved into 31 complete chromosomes and is paired with an assembled kinetoplast genome consisting of a maxicircle and 30 minicircle sequences. The assembly spans 33.7 Mb and contains very little repetitive content, from which our annotation of both the nuclear assembly and kinetoplast predicted 10,288 protein-coding genes. Analyses of the assembly revealed evidence of a recent chromosomal duplication event within chromosomes 5 and 6 and provides evidence for a high level of aneuploidy in this species, mirroring the genomic flexibility employed by other trypanosomatids as a means of adaptation to different environments. This high-quality reference can therefore provide insights into adaptations of trypanosomatids to the thermally regulated, acidic, and phytochemically rich honey bee hindgut niche, which offers parallels to the challenges faced by other Leishmaniinae during the challenges they undergo within insect vectors, during infection of mammals, and exposure to antiparasitic drugs throughout their multi-host life cycles. This reference will also facilitate investigations of strain-specific genomic polymorphisms, their role in pathogenicity, and the development of treatments for pollinator infection.

genomics↗

bioRxiv2023

High temperatures augment inhibition of parasites by a honey bee gut symbiont

Temperature affects growth, metabolism, and interspecific interactions in microbial communities. Within animal hosts, gut bacterial symbionts can provide resistance to parasitic infections. Infection can also be shaped by host body temperature. However, the effects of temperature on the antiparasitic activities of gut symbionts have seldom been explored. The Lactobacillus-rich gut microbiota of facultatively endothermic honey bees is subject to seasonal and ontogenetic changes in host temperature that could alter the effects of symbionts against parasites. We used cell cultures of a Lactobacillus symbiont and an important trypanosomatid gut parasite of honey bees to test the potential for temperature to shape parasite-symbiont interactions. We found that symbionts showed greater heat tolerance than parasites and chemically inhibited parasite growth via production of acids. Acceleration of symbiont growth and acid production at high temperatures resulted in progressively stronger antiparasitic effects across a temperature range typical of bee colonies. Consequently, the presence of symbionts reduced both peak growth rate and heat tolerance of parasites. Results suggest that the endothermic behavior of honey bees could potentiate the effectiveness of gut symbionts that limit parasites ability to withstand high temperature, implicating thermoregulation as a reinforcer of core symbioses and possibly microbiome-mediated antiparasitic defense. IMPORTANCETwo factors that shape the resistance of animals to infection are body temperature and gut microbiota. However, temperature can also alter interactions among microbes, raising the question of whether and how temperature changes the antiparasitic effects of gut microbiota. Honey bees are agriculturally important hosts of diverse parasites and infection-mitigating gut microbes. They can also socially regulate their body temperatures to an extent unusual for an insect. We show that high temperatures found in honey bee colonies augment the ability of a gut bacterial symbiont to inhibit growth of a common bee parasite and reduce the parasites ability to grow at high temperatures. This suggests that fluctuations in colony and body temperatures across life stages and seasons could alter the protective value of bees gut microbiota against parasites, and that temperature-driven changes in gut microbiota could be an underappreciated mechanism by which temperature-- including endothermy and fever-- alters animal infection.

ecology↗

bioRxiv2022

Host-driven temperature dependence of viral infection in honey bees

The temperature dependence of infection reflects changes in the performance of parasites and hosts. High temperatures (i.e., fever) often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit an endothermic, colony-level temperature regulation that is exceptional among insects and favors resistance to several parasites. However, proliferation of viruses is heavily host-dependent, suggesting that viral infection could be linked to--not threatened by--optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape virus proliferation, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied by <2-fold over a >30 {degrees}C interval that spanned the temperatures typical of ectothermic insects and honey bees. In contrast, metrics of honey bee performance peaked at high ([≥] 35 {degrees}C) temperatures and were highly temperature-sensitive, with respiration varying 8-fold over a 20 {degrees}C interval and successful development requiring a narrow 8 {degrees}C temperature range. Although these results suggested that hosts would gain a relative advantage over viruses with increasing temperature, the temperature dependence of pupal infection matched that of pupal development, falling only near pupaes upper thermal limits. Our results reflect the host-dependent nature of virus proliferation, suggesting that infection is accelerated--not curtailed--by optimum host function, contradicting predictions of infection based on the relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival. Despite a 98% reduction in infection at the upper end of the colony temperature range, the narrow thermal safety margin for honey bee development might preclude the effectiveness of fever for controlling viruses.

ecology↗

bioRxiv2021

Punch in the gut: Parasite tolerance of phytochemicals reflects host diet

Gut parasites of plant-eating insects are exposed to antimicrobial phytochemicals that can reduce infection. Trypanosomatid gut parasites infect insects of diverse nutritional ecologies as well as mammals and plants, raising the question of how host diet-associated phytochemicals shape parasite evolution and host specificity. To test the hypothesis that phytochemical tolerance of trypanosomatids reflects the chemical ecology of their hosts, we compared related parasites from honey bees and mosquitoes--hosts that differ in phytochemical consumption--and contrasted our results with previous studies on phylogenetically related, human-parasitic Leishmania. We identified one bacterial and ten plant-derived substances with known antileishmanial activity that also inhibited honey bee parasites associated with colony collapse. Bee parasites exhibited greater tolerance of chrysin--a flavonoid found in nectar, pollen, and plant resin-derived propolis. In contrast, mosquito parasites were more tolerant of cinnamic acid--a product of lignin decomposition present in woody debris-rich larval habitats. Parasites from both hosts tolerated many compounds that inhibit Leishmania, hinting at possible trade-offs between phytochemical tolerance and mammalian infection. Our results implicate the phytochemistry of host diets as a potential driver of insect-trypanosomatid associations, and identify compounds that could be incorporated into colony diets or floral landscapes to ameliorate infection in bees. ORIGINALITY AND SIGNIFICANCETrypanosomatid parasites of insects pose threats to beneficial insects, crop plants, and human health. Elucidation of the environmental factors that determine host-parasite specificity and transmission of trypanosomatids is essential to predict the spread and spillover potential of trypanosomatids in wild and agricultural ecosystems. Our comparisons between trypanosomatids of bees and mosquitoes implicate the phytochemical composition of host diets as a potential determinant of insect-trypanosomatid associations. To our knowledge, this is the first comparative study of phytochemical tolerance in insect trypanosomatids. As the first characterization of phytochemical tolerance among honey bee-associated trypanosomatids, our results also identify compounds that could ameliorate infection of managed bees with parasites of concern to wild pollinators and associated with colony collapse.

ecology↗

bioRxiv2021

Mites alight! Sunflower crop area and pollen supplementation enhance honey bee resistance to Varroa destructor

Anthropogenic landscape changes can affect parasite epidemiology in wild and agricultural animals. Honey bees are agricultural animals whose services are threatened by loss of floral resources and by parasites, most notably the invasive mite Varroa destructor. Existing mite control strategies rely heavily on chemical treatments that can adversely affect bees. Alternative, pesticide-free control methods are urgently needed to maintain effective pollination services. Many flowering plants provide nectar and pollen that enhance resistance to parasites in animals. Enrichment of landscapes with antiparasitic floral resources could therefore provide a sustainable means of parasite control in pollinators. Floral rewards of Asteraceae plants have been shown to reduce parasitic infection in diverse bee species, including honey and bumble bees. Here, we tested the effects of sunflower (Helianthus annuus) cropland and pollen supplementation on honey bee resistance to macro- and microparasites. Our results show that each doubling of sunflower crop area is associated with a 28% reduction in mite infestation intensity. Late-summer supplementation of colonies with sunflower pollen reduced mite infestation by 2.75-fold relative to an artificial pollen. Our findings suggest the potential for sunflower plantings or pollen supplements to counteract a main driver of honey bee losses worldwide.

ecology↗

bioRxiv2021

Hot and sour: parasite adaptations to honey bee body temperature and pH

Host temperature and gut chemistry can shape resistance to parasite infection. Heat and acidity can limit trypanosomatid infection in warm-blooded hosts, and could shape infection resistance in insects as well. The colony-level endothermy and acidic guts of social bees provide unique opportunities to study how temperature and acidity shape insect-parasite associations. We compared temperature and pH tolerance between three trypanosomatid parasites from social bees and a related trypanosomatid from poikilothermic mosquitoes, which have alkaline guts. Relative to the mosquito parasites, all three bee parasites had higher heat tolerance that reflected levels of endothermy in hosts. Heat tolerance of the honey bee parasite Crithidia mellificae was exceptional for its genus, implicating honey bee endothermy as a filter of parasite establishment. The lesser heat tolerance of the emerging Lotmaria passim suggests possible spillover from a less endothermic host. Whereas both honey bee parasites tolerated the acidic pHs found in bee intestines, mosquito parasites tolerated the alkaline conditions found in mosquito midguts, suggesting that both gut pH and temperature could structure host-parasite specificity. Elucidating how host temperature and gut pH affect infection--and corresponding parasite adaptations to these factors--could help explain trypanosomatids distribution among insects and invasion of mammals.

ecology↗

bioRxiv2021

Beeporter: a high-throughput tool for non-invasive analysis of honey bee virus infection

Honey bees face numerous pests and pathogens but arguably none are as devastating as Deformed wing virus (DWV). Development of antiviral therapeutics and virus-resistant honey bee lines to control DWV in honey bees is slowed by the lack of a cost-effective high-throughput screening of DWV infection. Currently, analysis of virus infection and screening for antiviral treatments in bees and their colonies is tedious, requiring a well-equipped molecular biology laboratory and the use of hazardous chemicals. Here we utilize a cDNA clone of DWV tagged with green fluorescent protein (GFP) to develop the Beeporter assay, a method for detection and quantification of DWV infection in live honey bees. The assay involves infection of honey bee pupae by injecting a standardized DWV-GFP inoculum, followed by incubation for up to 44 hours. GFP fluorescence is recorded at intervals via commonly available long-wave UV light sources and a smartphone camera or a standard ultraviolet transilluminator gel imaging system. Nonlethal DWV monitoring allows high-throughput screening of antiviral candidates and a direct breeding tool for identifying honey bee parents with increased antivirus resistance. For even more rapid drug screening, we also describe a method for screening bees using 96-well trays and a spectrophotometer.

microbiology↗

bioRxiv2018

Temperature-mediated inhibition of a bumble bee parasite by an intestinal symbiont

Competition between organisms is often mediated by environmental factors including temperature. In animal intestines, nonpathogenic symbionts compete physically and chemically against pathogens, with consequences for host infection. We used metabolic theory-based models to characterize differential responses to temperature of a bacterial symbiont and a co-occurring trypanosomatid parasite of bumble bees, which regulate body temperature during flight and incubation. We hypothesized that inhibition of parasites by bacterial symbionts would increase with temperature, due to symbionts having higher optimal growth temperatures than parasites.\n\nWe found that a temperature increase over the range measured in bumble bee colonies would favor symbionts over parasites. As predicted by our hypothesis, symbionts reduced the optimal growth temperature for parasites, both in direct competition and when parasites were exposed to symbiont spent medium. Inhibitory effects of the symbiont increased with temperature, reflecting accelerated growth and acid production by symbionts. Our results indicate that high temperatures, whether due to host endothermy or environmental factors, can enhance the inhibitory effects of symbionts on parasites. Temperature-modulated manipulation of microbiota could be one explanation for fever- and heat-induced reductions of infection in animals, with consequences for diseases of medical and conservation concern.

ecology↗

bioRxiv2018

pH-mediated inhibition of a bumble bee parasite by an intestinal symbiont

Non-pathogenic microbes can provide multiple benefits to their hosts, including pathogen inhibition. Gut symbionts can augment resistance to pathogens by stimulating host immune responses, competing for space and nutrients, or producing antimicrobial metabolites. The gut microbiota of social bees, which pollinate many crops and wildflowers, has demonstrated benefits against diverse infections and might help protect against pathogen-related declines. The bumble bee gut microbiota, consisting chiefly of five taxa common to corbiculate bees, has been shown to enhance resistance to the trypanosomatid parasite Crithidia bombi. Specifically, infection intensity was negatively correlated with abundance of Lactobacillus \"Firm-5\" bacteria. However, the mechanism underlying this relationship remains unknown. We tested the hypothesis that the Firm-5 bacterium Lactobacillus bombicola, which produces lactic acid, inhibits C. bombi via a pH-mediated effect.\n\nConsistent with our hypothesis, Lactobacillus bombicola spent medium inhibited C. bombi growth via a reduction in pH that was both necessary and sufficient for inhibition. Inhibition of all parasite strains occurred within the pH range previously observed in honey bee guts, though sensitivity to acidity varied among parasite strains. Spent medium was slightly more potent than HCl, D-, and L-lactic acids for a given pH, suggesting that other metabolites also contribute to inhibitory effects. Our results implicate symbiont-mediated reduction in gut pH as a key determinant of trypanosomatid infection in bees. Future investigation into in vivo effects of gut microbial composition on pH and infection intensity would help determine the relevance of these findings for bees threatened by trypanosomatids.\n\nImportancePollinators such as honey and bumble bees provide services to plants in agricultural and wild ecosystems, but both wild and managed bees are threatened by infection-related declines. The symbiotic gut microbiota of bees provides a naturally occurring defense against infection. For example, the bumble bee microbiota reduces infection with trypanosomatid parasites, but how inhibition occurs remains unknown. We show that the acidic spent medium from a common bumble bee gut symbiont, Lactobacillus bombicola, inhibits in vitro growth of the trypanosomatid gut parasite, Crithidia bombi. The acidity of the spent medium was both necessary and sufficient for parasite inhibition. Inhibitory pH values were within the range documented in honey bee guts, suggesting that pH-mediated parasite inhibition is plausible in live bees. Results suggest that production of acids by sugar-fermenting symbionts confers pH-mediated resistance to infection in bees, whereas depletion of core microbiota could result in low-acid conditions that favor parasite growth.

ecology↗