Thermal niches of specialized gut symbionts: the case of social bees

Responses to climate change are particularly complicated in species that engage in symbioses, as the niche of one partner may be modified by that of the other. We explored thermal traits in gut symbionts of honeybees and bumblebees, which are vulnerable to rising temperatures. In vitro assays of symbiont strains isolated from 16 host species revealed variation in thermal niches. Strains from bumblebees tended to be less heat-tolerant than those from honeybees, possibly due to bumblebees maintaining cooler nests or inhabiting cooler climates. Overall, however, bee symbionts grew at temperatures up to 44°C and withstood temperatures up to 52°C, at or above the upper thermal limits of their hosts. While heat-tolerant, most strains of the symbiont Snodgrassella grew relatively slowly below 35°C, perhaps because of adaptation to the elevated body temperatures that bees maintain through thermoregulation. In a gnotobiotic bumblebee experiment, Snodgrassella was unable to consistently colonize bees reared at 29°C under conditions that limit thermoregulation. Thus, host thermoregulatory behaviour appears important in creating a warm microenvironment for symbiont establishment. Bee–microbiome–temperature interactions could affect host health and pollination services, and inform research on the thermal biology of other specialized gut symbionts.

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Thermal niches of specialized gut symbionts: the case of social bees

10.1101/2020.06.16.155309 ◽

2020 ◽

Author(s):

Tobin J. Hammer ◽

Eli Le ◽

Nancy A. Moran

Keyword(s):

Thermoregulatory Behavior ◽

Pollination Services ◽

Thermal Biology ◽

Social Bees ◽

Thermal Limits ◽

Host Health ◽

Gut Symbionts ◽

Heat Tolerant ◽

Temperature Interactions

AbstractResponses to climate change are particularly complicated in species that engage in symbioses, as the niche of one partner may be modified by that of the other. We explored thermal traits in gut symbionts of honeybees and bumblebees, which are vulnerable to rising temperatures. In vitro assays of symbiont strains isolated from 16 host species revealed variation in thermal niches. Strains from bumblebees tended to be less heat-tolerant than those from honeybees, possibly due to bumblebees maintaining cooler nests or inhabiting cooler climates. Overall however, bee symbionts grew at temperatures up to 44 °C and withstood temperatures up to 52 °C, at or above the upper thermal limits of their hosts. While heat-tolerant, most strains of the symbiont Snodgrassella grew relatively slowly below 35 °C, perhaps because of adaptation to the elevated body temperatures that bees maintain through thermoregulation. In a gnotobiotic bumblebee experiment, Snodgrassella was unable to consistently colonize bees reared below 35 °C under conditions that limit thermoregulation. Thus, host thermoregulatory behavior appears important in creating a warm microenvironment for symbiont establishment. Bee-microbiome-temperature interactions could affect host health and pollination services, and inform research on the thermal biology of other specialized gut symbionts, such as those of humans.

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Immune system stimulation by the native gut microbiota of honey bees

Royal Society Open Science ◽

10.1098/rsos.170003 ◽

2017 ◽

Vol 4 (2) ◽

pp. 170003 ◽

Cited By ~ 105

Author(s):

Waldan K. Kwong ◽

Amanda L. Mancenido ◽

Nancy A. Moran

Keyword(s):

Immune System ◽

Gut Microbiota ◽

Honey Bee ◽

E Coli ◽

Crucial Component ◽

Host Health ◽

Gut Symbionts ◽

Microbial Symbionts ◽

Insect Innate Immunity

Gut microbial communities can greatly affect host health by modulating the host's immune system. For many important insects, however, the relationship between the gut microbiota and immune function remains poorly understood. Here, we test whether the gut microbial symbionts of the honey bee can induce expression of antimicrobial peptides (AMPs), a crucial component of insect innate immunity. We find that bees up-regulate gene expression of the AMPs apidaecin and hymenoptaecin in gut tissue when the microbiota is present. Using targeted proteomics, we detected apidaecin in both the gut lumen and the haemolymph; higher apidaecin concentrations were found in bees harbouring the normal gut microbiota than in bees lacking gut microbiota. In in vitro assays, cultured strains of the microbiota showed variable susceptibility to honey bee AMPs, although many seem to possess elevated resistance compared to Escherichia coli . In some trials, colonization by normal gut symbionts resulted in improved survivorship following injection with E. coli . Our results show that the native, non-pathogenic gut flora induces immune responses in the bee host. Such responses might be a host mechanism to regulate the microbiota, and could potentially benefit host health by priming the immune system against future pathogenic infections.

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Intracellular pH-temperature interactions of hepatocytes from American eels

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1983.245.1.r32 ◽

1983 ◽

Vol 245 (1) ◽

pp. R32-R37

Author(s):

P. J. Walsh ◽

T. W. Moon

Keyword(s):

Intracellular Ph ◽

Acclimation Temperature ◽

C Cells ◽

Medium Ph ◽

American Eel ◽

Temperature Changes ◽

American Eels ◽

Temperature Interactions

The effects of acclimation temperature and acute temperature changes on the intracellular pH (pHi) of hepatocytes isolated from the American eel, Anguilla rostrata, were studied by the measurement of the distribution ratio of dimethyloxizolidinedione (DMO). Varying the concentration of DMO (10(-7) to 10(-4) M) did not affect estimates of pHi, indicating that DMO acts as an ideal pHi probe in eel hepatocytes. In vitro studies yielded values of liver cell pHi identical to those previously measured in vivo (in vitro pHi = 7.556 +/- 0.010; in vivo pHi = 7.570 +/- 0.049 at 20 degrees C); hepatocyte pHi varied inversely with acclimation temperature (5-20 degrees C) in a manner consistent with alphastat regulation (delta pH/delta T = -0.0182 +/- 0.021). During acute temperature increases (5-20 degrees C) and decreases (20-5 degrees C) hepatocytes regulated pHi to the appropriate (acclimated) value within 30-45 min posttransfer under conditions of constant medium pH (pHe). The effects of medium pH were also studied, and although patterns of pHi regulation differed between 5 and 20 degrees C cells, a pHi difference consistent with alphastat regulation was maintained between 5 and 20 degrees C cells over the pHe range 7.8-8.3.

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In vitro assessment of histamine and lactate production by a multi-strain synbiotic

Journal of Food Science and Technology ◽

10.1007/s13197-021-05327-7 ◽

2021 ◽

Author(s):

Gerrit Stuivenberg ◽

Brendan Daisley ◽

Polycronis Akouris ◽

Gregor Reid

Keyword(s):

Lactic Acidosis ◽

Lactate Production ◽

Fermented Food ◽

In Vitro Production ◽

Food Items ◽

Host Health ◽

In Vitro Assessment ◽

Vitro Production ◽

Significant Production

AbstractRecent studies suggest histamine and d-lactate may negatively impact host health. As excess histamine is deleterious to the host, the identification of bacterial producers has contributed to concerns over the consumption of probiotics or live microorganisms in fermented food items. Some probiotic products have been suspected of inducing d-lactic-acidosis; an illness associated with neurocognitive symptoms such as ataxia. The goals of the present study were to test the in vitro production of histamine and d-lactate by a 24-strain daily synbiotic and to outline methods that others can use to test for their production. Using enzymatic based assays, no significant production of histamine was observed compared to controls (P > 0.05), while d-lactate production was comparable to a commercially available probiotic with no associated health risk. These assays provide a means to add to the safety profile of synbiotic and probiotic products.

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Higher Variability in Fungi Compared to Bacteria in the Foraging Honey Bee Gut

10.1101/2020.10.20.348128 ◽

2020 ◽

Author(s):

Leslie E. Decker ◽

Priscilla A. San Juan ◽

Magdalena L. Warren ◽

Cory E. Duckworth ◽

Cheng Gao ◽

...

Keyword(s):

Species Composition ◽

Microbial Communities ◽

Honey Bee ◽

Honey Bees ◽

Plant Pathogens ◽

Distribution Patterns ◽

Model System ◽

Pathogen Transmission ◽

Host Health ◽

Gut Symbionts

AbstractMicrobial communities in the honey bee gut have emerged as a model system to understand the effects of host-associated microbes on animals and plants. The specific distribution patterns of bacterial associates among honey bee gut regions remains a key finding within the field. The mid- and hindgut of foraging bees house a deterministic set of core species that affect host health. In contrast, the crop, or honey stomach, contains a more diverse set of bacteria that is highly variable in composition among individual bees. Whether this contrast between the two gut regions also applies to fungi, another major group of gut-associated microbes, remains unclear despite their potential influence on host health. In honey bees caught foraging at four sites across the San Francisco Peninsula, we found that fungi were much less distinct in species composition between the crop and the mid- and hindgut than bacteria. Unlike bacteria, fungi were highly variable in composition throughout the gut, and much of this variation was attributable to bee collection site. These patterns suggest that the fungi may be passengers rather than functionally significant gut symbionts. However, many of the fungi we found in the bees have been recognized as plant pathogens. Assuming that some fungi remain viable after passage through the gut, the distribution patterns we report here point to the potential importance of honey bees as vectors of fungal pathogens and suggest a more prominent role of honey bees in plant pathogen transmission than generally thought.Importance (Nontechnical explanation of why the work was undertaken)Along with bacteria, fungi make up a significant portion of animal- and plant-associated microbial communities. However, we have only begun to describe these fungi, much less examine their effects on most animals and plants. The honey bee, Apis mellifera, has emerged as a model system for studying host-associated microbes. Honey bees contain well-characterized bacteria specialized to inhabit different regions of the gut. Fungi also exist in the honey bee gut, but their composition and function remain largely undescribed. Here we show that, unlike bacteria, fungi vary substantially in species composition throughout the honey bee gut, contingent on where the bees are sampled. This observation suggests that fungi may be transient passengers and therefore unimportant as gut symbionts. However, our findings also indicate that honey bees could be major vectors of infectious plant diseases as many of the fungi we found in the honey bee gut are recognized as plant pathogens.

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Regulation mode of evaporative cooling underlying a strategy of the heat-tolerant FOK rat for enduring ambient heat

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.00198.2003 ◽

2003 ◽

Vol 285 (6) ◽

pp. R1439-R1445 ◽

Cited By ~ 5

Author(s):

Fujiya Furuyama ◽

Masataka Murakami ◽

Etsuro Tanaka ◽

Hideki Hida ◽

Daisuke Miyazawa ◽

...

Keyword(s):

Heat Tolerance ◽

Strain Difference ◽

Strain Differences ◽

Ambient Temperatures ◽

Saliva Secretion ◽

Wide Range ◽

Heat Tolerant ◽

Hot Environments ◽

Regulation Mode

Compared with other rat strains, the inbred FOK rat is extremely heat tolerant. This increased heat tolerance is due largely to the animal's enhanced saliva spreading abilities. The aims of the present study were to 1) quantify the heat tolerance capacity of FOK rats and 2) determine the regulatory mode of the enhanced salivary cooling in these animals. Various strains of rats were acutely exposed to heat. In the heat-intolerant strains, saliva spreading was insufficient and the core temperature (Tc) rose rapidly. In contrast, FOK rats maintained an elevated Tc plateau (39.5 ± 0.7°C) for 5-6 h over a wide range of ambient temperatures (Ta) (37.5-42.5°C). In hot environments the FOK rats secreted copious amounts of saliva and spread it over more than the entire ventral body surface. FOK rats had a low Tc threshold for salivation, and the salivation rate increased linearly in proportion to the Tc deviation from the threshold. No strain difference or temperature effect was observed in the saliva secretion rate from in vitro submandibular glands perfused by sufficient doses of ACh. These results suggest that 1) the ability of FOK rats to maintain a moderate steady-state hyperthermia (39.5 ± 0.7°C) over a wide Ta range is enabled by a lowered threshold Tc for salivation and functional negative-feedback control of saliva secretion and 2) strain differences in ability to endure heat stress are mainly attributable to changes in the thermoregulatory control system rather than altered secretory abilities of the salivary glands.

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The swift parrot Lathamus discolor (Psittacidae), social bees (Apidae), and native insects as pollinators of Eucalyptus globulus ssp. globulus (Myrtaceae)

Australian Journal of Botany ◽

10.1071/bt03018 ◽

2004 ◽

Vol 52 (3) ◽

pp. 371 ◽

Cited By ~ 32

Author(s):

A. B. Hingston ◽

B. M. Potts ◽

P. B. McQuillan

Keyword(s):

Eucalyptus Globulus ◽

Seed Set ◽

Bombus Terrestris ◽

Pollination Services ◽

Social Bees ◽

Single Flower ◽

Fitness Benefits ◽

The Cost ◽

Effective Pollinator ◽

Better Than

It has been argued that the production of sufficient nectar to attract bird pollinators would evolve if the fitness benefits accruing from pollination services by birds, compared with insects, outweighed the cost of increased allocation of photosynthate to nectar. This hypothesis implies that the pollination services provided by birds must be considerably better than those provided by insects with which the plant has evolved. Consistent with this, we found that the endangered native swift parrot Lathamus discolor (Shaw) was a very effective pollinator of the native tree Eucalyptus globulus Labill. in Tasmania, facilitating an average of 76% of the maximum possible seed set for open-pollinated flowers in just one visit to a flower, whereas single flower visits by native insects did not facilitate any seed production. Flowers visited once by either species of introduced social bees, the honeybee Apis mellifera L. or the bumblebee Bombus terrestris (L.), produced less than 7% of the maximum possible seed set for open-pollinated flowers. Hence, easily managed social bees appear to be poor substitutes for bird pollinators in commercial seed orchards of this tree. We propose three possible reasons why this largely bird-pollinated tree has not evolved characters that deter insects from removing nectar.

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Prebiotics from Seaweeds: An Ocean of Opportunity?

Marine Drugs ◽

10.3390/md17060327 ◽

2019 ◽

Vol 17 (6) ◽

pp. 327 ◽

Cited By ~ 23

Author(s):

Paul Cherry ◽

Supriya Yadav ◽

Conall R. Strain ◽

Philip J. Allsopp ◽

Emeir M. McSorley ◽

...

Keyword(s):

Fatty Acids ◽

Gut Microbiota ◽

Animal Studies ◽

Health Benefit ◽

Microbial Composition ◽

Previous Discussion ◽

Host Health ◽

Health Related

Seaweeds are an underexploited and potentially sustainable crop which offer a rich source of bioactive compounds, including novel complex polysaccharides, polyphenols, fatty acids, and carotenoids. The purported efficacies of these phytochemicals have led to potential functional food and nutraceutical applications which aim to protect against cardiometabolic and inflammatory risk factors associated with non-communicable diseases, such as obesity, type 2 diabetes, metabolic syndrome, cardiovascular disease, inflammatory bowel disease, and some cancers. Concurrent understanding that perturbations of gut microbial composition and metabolic function manifest throughout health and disease has led to dietary strategies, such as prebiotics, which exploit the diet-host-microbe paradigm to modulate the gut microbiota, such that host health is maintained or improved. The prebiotic definition was recently updated to “a substrate that is selectively utilised by host microorganisms conferring a health benefit”, which, given that previous discussion regarding seaweed prebiotics has focused upon saccharolytic fermentation, an opportunity is presented to explore how non-complex polysaccharide components from seaweeds may be metabolised by host microbial populations to benefit host health. Thus, this review provides an innovative approach to consider how the gut microbiota may utilise seaweed phytochemicals, such as polyphenols, polyunsaturated fatty acids, and carotenoids, and provides an updated discussion regarding the catabolism of seaweed-derived complex polysaccharides with potential prebiotic activity. Additional in vitro screening studies and in vivo animal studies are needed to identify potential prebiotics from seaweeds, alongside untargeted metabolomics to decipher microbial-derived metabolites from seaweeds. Furthermore, controlled human intervention studies with health-related end points to elucidate prebiotic efficacy are required.

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Microbial Ecology of European Foul Brood Disease in the Honey Bee (Apis mellifera): Towards a Microbiome Understanding of Disease Susceptibility

Insects ◽

10.3390/insects11090555 ◽

2020 ◽

Vol 11 (9) ◽

pp. 555

Author(s):

Amy S. Floyd ◽

Brendon M. Mott ◽

Patrick Maes ◽

Duan C. Copeland ◽

Quinn S. McFrederick ◽

...

Keyword(s):

Apis Mellifera ◽

Disease Transmission ◽

Larval Survival ◽

Limited Attention ◽

Pollination Services ◽

Bacterial Microbiota ◽

Probiotic Treatment ◽

Colony Loss ◽

Negative Controls

European honey bees (Apis mellifera Linnaeus) are beneficial insects that provide essential pollination services for agriculture and ecosystems worldwide. Modern commercial beekeeping is plagued by a variety of pathogenic and environmental stressors often confounding attempts to understand colony loss. European foulbrood (EFB) is considered a larval-specific disease whose causative agent, Melissococcus plutonius, has received limited attention due to methodological challenges in the field and laboratory. Here, we improve the experimental and informational context of larval disease with the end goal of developing an EFB management strategy. We sequenced the bacterial microbiota associated with larval disease transmission, isolated a variety of M.plutonius strains, determined their virulence against larvae in vitro, and explored the potential for probiotic treatment of EFB disease. The larval microbiota was a low diversity environment similar to honey, while worker mouthparts and stored pollen contained significantly greater bacterial diversity. Virulence of M. plutonius against larvae varied markedly by strain and inoculant concentration. Our chosen probiotic, Parasaccharibacter apium strain C6, did not improve larval survival when introduced alone, or in combination with a virulent EFB strain. We discuss the importance of positive and negative controls for in vitro studies of the larval microbiome and disease.

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