Colonization of Honey Bee Digestive Tracts by Environmental Yeast
            <i>Lachancea thermotolerans</i>
            Is Naturally Occurring, Temperature Dependent, and Impacts the Microbiome of Newly Emerged Bees

Kogan, Helen V.; Elikan, Annabelle B; Glaser, Kimberly F; Bergmann, Jenna M.; Raymond, Laure M; Prado-Irwin, Sofia R.; Snow, Jonathan W.

doi:10.1128/spectrum.05194-22

Cited by 6 publications

(5 citation statements)

References 83 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The manipulability of both microbiome and body temperature in a host with a predominantly endothermic life history strategy makes honey bees a useful system to explore the value of endothermy as a reinforcer of symbioses and symbiont-mediated defense against parasites. Prior work has shown that high (35 °C) temperatures increase resistance of honey bees to colonization by heat-sensitive environmental yeasts relative to cooler (29 °C) temperatures, consistent with the seasonal appearance of yeasts during colder weather in field-collected forager bees (73). On the other hand, high (35 °C) temperatures enhanced growth of and gut colonization by the core symbiont S. alvi in bumble bees relative to low (28-29 °) temperatures (64).…”

Section: Discussionsupporting

confidence: 63%

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

Palmer‐Young¹,

Markowitz

Huang³

et al. 2023

Preprint

View full text Add to dashboard Cite

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 parasite ability to withstand high temperature, implicating thermoregulation as a reinforcer of core symbioses and possibly microbiome-mediated antiparasitic defense. Importance: Two 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 parasite&#39s 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&#39 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.

show abstract

Section: Discussionsupporting

confidence: 63%

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

Palmer‐Young¹,

Markowitz

Huang³

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…To determine whether bleomycin treatment impacts the microbiome, we used primer sets amplifying the 16S rRNA region of all bacteria as well as sets that amplify the species-specific 16S rRNA region of the most predominant species in uninoculated cage-reared bees, Gilliamella apicola ( 19 ). Combining the data from three independent trials, we found that bleomycin (0.613 µg/mL) had no statistically significant effect on total bacteria levels or on the levels of G. apicola in the midgut ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…For examining levels of total bacteria and one specific bacterial species of the digestive tract microbiome ( Gilliamella apicola ), a similar assay was performed using universal 16S rRNA primers and species-specific 16S rRNA primers from reference ( 18 ) in conjunction with the honey bee ATP5a gene. G. apicola was chosen as the single bacterial species to investigate in more detail because previous studies have found that this is the predominant species in uninoculated cage-reared bees ( 19 , 20 ), while other bacterial subsets are typically highly variable and at very low levels.…”

Section: Methodsmentioning

confidence: 99%

Bleomycin reduces Vairimorpha (Nosema) ceranae infection in honey bees with some evident host toxicity

Parrella,

Elikan,

Kogan

et al. 2024

Microbiol Spectr

Self Cite

View full text Add to dashboard Cite

Microsporidia cause disease in many beneficial insects, including honey bees, yet few pathogen control tools are available for protecting these important organisms against infection. Some evidence suggests that microsporidia possess a reduced number of genes encoding DNA repair proteins. We hypothesized that microsporidia would thus be susceptible to treatment with DNA-damaging agents and tested this hypothesis using a novel, rapid method for achieving robust and homogenous experimental infection of large numbers of newly emerged honey bees with one of its microsporidia pathogens, Vairimorpha ( Nosema ) ceranae . In carrying out these experiments, we found this novel V. ceranae inoculation method to have similar efficacy as other traditional methods. We show that the DNA-damaging agent bleomycin reduces V. ceranae levels, with minimal but measurable effects on honey bee survival and increased expression of midgut cellular stress genes, including those encoding SHSP. Increased expression of UpdlC suggests the occurrence of epithelial regeneration, which may contribute to host resistance to bleomycin treatment. While bleomycin does reduce infection levels, host toxicity issues may preclude its use in the field. However, with further work, bleomycin may provide a useful tool in the research setting as a potential selection agent for genetic modification of microsporidia. IMPORTANCE Microsporidia cause disease in many beneficial insects, yet there are few tools available for control in the field or laboratory. Based on the reported paucity of DNA repair enzymes found in microsporidia genomes, we hypothesized that these obligate intracellular parasites would be sensitive to DNA damage. In support of this, we observed that the well-characterized DNA damage agent bleomycin can reduce levels of the microsporidia Vairimorpha ( Nosema ) ceranae in experimental infections in honey bees. Observation of slightly reduced honey bee survival and evidence of sublethal toxicity likely preclude the use of bleomycin in the field. However, this work identifies bleomycin as a compound that merits further exploration for use in research laboratories as a potential selection agent for generating genetically modified microsporidia.

show abstract

“…We highlight the better performance of wild strains at low temperatures, which may improve survival in wild environments such as those associated with insects or subboreal locations (Hranilovic et al, 2017). It has been verified that colonization of bee digestive tracts by L. thermotolerans is associated with lower temperatures (Kogan et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

Whole-genome sequencing and phenotyping reveal specific adaptations ofLachancea thermotoleransto the winemaking environment

Vicente,

Friedrich,

Schacherer

et al. 2024

Preprint

View full text Add to dashboard Cite

Adaptation to the environment plays an essential role in yeast evolution as a consequence of selective pressures.Lachancea thermotolerans, a yeast related to the fermentative process and one of the current trends in wine technology research, has undergone an anthropization process that has led to a strong differentiation both from a genomic and phenomic perspective. Using whole-genome sequencing, we have investigated the genomic diversity of 145L. thermotoleransstrains, identifying six well-defined groups primarily delineated by their ecological origin and exhibiting high levels of genetic diversity. Anthropized strains showed lower genetic diversity due to the purifying selection imposed by the winemaking environment. Strong evidence of anthropization and adaptation to the wine environment through modification of gene content was also found. Differences in genes involved in the assimilation of alternative carbon and nitrogen sources, such as theMAL1andDAL5genes, which confer greater fitness in the winemaking environment, were observed. Additionally, we found that phenotypic traits considered domestication hallmarks are present in anthropized strains. Among these, increased fitness in the presence of ethanol and sulphites, assimilation of non-fermentable carbon sources such as glycerol, and lower levels of residual fructose under fermentative conditions highlight. We hypothesize that lactic acid production by wine-related strains is an anthropization signature consequence of the adaption of early Crabtree-positive yeasts to the fermentative environment. Overall, the results of this work provide valuable insight into the anthropization process inL. thermotoleransand demonstrate how fermentation environments give rise to similar adaptations in different yeast species.

show abstract

Colonization of Honey Bee Digestive Tracts by Environmental Yeast Lachancea thermotolerans Is Naturally Occurring, Temperature Dependent, and Impacts the Microbiome of Newly Emerged Bees

Cited by 6 publications

References 83 publications

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

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

Bleomycin reduces Vairimorpha (Nosema) ceranae infection in honey bees with some evident host toxicity

Whole-genome sequencing and phenotyping reveal specific adaptations ofLachancea thermotoleransto the winemaking environment

Contact Info

Product

Resources

About