<i>Apis cerana</i>gut microbiota contribute to host health though stimulating host immune system and strengthening host resistance to<i>Nosema ceranae</i>

Wu, Yuqi; Zheng, Yi; Chen, Yanan; Chen, Gongwen; Zheng, Huoqing; Hu, Fuliang

doi:10.1098/rsos.192100

Cited by 28 publications

(23 citation statements)

References 47 publications

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“…4), which are common opportunistic bacterial pathogens in insects (81,82). Adult butterflies may be similar to pyrrhocorid bugs, tsetse flies and social bees, in which gut bacteria provide an important layer of defense against related parasites and pathogens (83)(84)(85)(86)(87). Importantly, colonization resistance can readily evolve even in symbioses lacking strong host-microbe specificity (88), such as that between heliconiines and their adult-stage microbiomes.…”

Section: Discussionmentioning

confidence: 99%

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

Hammer

Dickerson

McMillan

et al. 2019

Preprint

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1 2 Evolutionary transitions in animal diets often coincide with shifts in the microbiome, but 3 the degree to which diet-microbiome feedbacks vary across host taxa and development is 4 unresolved. We examined these potential feedbacks from the perspective of Lepidoptera 5 (butterflies and moths), a diverse clade in which little is known about adult-stage microbial 6 associations. With the exception of Heliconius butterflies, most lepidopteran adults are short-7 lived and either feed on simple substrates, like nectar, or do not feed at all. Heliconius consume 8 pollen as adults, which provides amino acids and allows the butterflies to have an extended 9 lifespan. Using 16S rRNA gene sequencing of 214 field-collected individuals, we found that 10 adult passion-vine butterfly microbiomes exhibited a strong signal of host phylogeny, with a 11 clear distinction between Heliconius and non-pollen-feeding relatives. This pattern was largely 12 driven by differing relative abundances of bacterial phylotypes shared among host taxa, as 13 opposed to the presence or absence of host-specific phylotypes. Using shotgun metagenomic 14 sequencing, we also discovered trypanosomatids and microsporidia to be prevalent in butterfly 15 guts, suggesting potential interactions with co-localized gut bacteria. Overall, we show that a 16 major transition in adult-stage lepidopteran diet and life history coincides with a shift in 17 microbiomes, and our work provides a foundation for future tests of microbiome function in 18 adult butterflies. 19 20 Lepidoptera (butterflies and moths) are a diverse and ecologically important group in 31 which microbiome roles are likely to be highly specific to certain host taxa and life stages. For 32 lepidopteran larvae (caterpillars), even major shifts in larval diet do not coincide with 33 functionally relevant shifts in the microbiome [9][10][11]. Lepidopteran larvae typically harbor a 34 very low number of gut microbes, and most of these microbes are transient with the exception of 35 pathogen infections [9]. However, the microbiomes of insects that undergo complete 36 metamorphosis, such as Lepidoptera, often exhibit profound shifts in size, composition and 37 function across host life stages [7]. A recent survey of various butterfly species found that adult-38 stage gut bacterial communities were generally abundant (median ~10 8 16S rRNA gene copies 39 per gut) and distinct from diet-associated bacterial communities [12]. It is possible that 40 evolutionary transitions in the diet of adult lepidopterans could cause, or be caused by, 41 concomitant transitions in adult-stage microbiomes. 42Arguably, the single most dramatic and consequential transition in adult diet among the 43 150,000+ described species of Lepidoptera [13] occurred in the ancestors of neotropical 44Heliconius butterflies (Nymphalidae: Heliconiini). While adults of other lepidopterans either do 45 not feed at all, or feed on comparatively nitrogen-poor and/or inconsistently available substrates 46 [14], Heliconius evolved the abili...

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Section: Discussionmentioning

confidence: 99%

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

Hammer

Dickerson

McMillan

et al. 2019

Preprint

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“…Bacterial loads of workers were determined by quantitative PCR (qPCR) using universal bacterial 16S rRNA primers (F: 5′-AGAGTTTGATCCTGGCTCAG-3,′ R: 5′-CTGCTGCCTCCCGTAGGAGT-3′). Sampled guts of workers were obtained according to the protocol described by Wu et al (2020a) and their DNA using TIANamp Stool DNA Kit (Tiangen Biotech Co., Ltd., Beijing, China) according to the manufacturer’s protocol. The StepOne Plus real time PCR system was used for the absolute quantification of 16S rRNA copy number.…”

Section: Methodsmentioning

confidence: 99%

The Pass-on Effect of Tetracycline-Induced Honey Bee (Apis mellifera) Gut Community Dysbiosis

Jia

Chen

et al. 2022

Front. Microbiol.

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Gut microbial community plays an important role in the regulation of insect health. Antibiotic treatment is powerful to fight bacterial infections, while it also causes collateral damage to gut microbiome, which may have long-lasting consequences for host health. However, current studies on honey bees mainly focus on the impact of direct exposure to antibiotics on individual bees, and little is known about the impact of social transmission of antibiotic-induced gut community disorder in honey bee colonies. In order to provide insight into the potential pass-on effect of antibiotic-induced dysbiosis, we colonized newly emerged germ-free workers with either normal or tetracycline-treated gut community and analyzed the gut bacteria composition. We also treated workers with low dosage of tetracycline to evaluate its impact on honey bee gut microbiota. Our results showed that the tetracycline-treated gut community caused disruption of gut community in their receivers, while the direct exposure to the low dosage of tetracycline had no significant effect. In addition, no significant difference was observed on the mortality rate of A. mellifera workers with different treatments. These results suggest that though the residue of antibiotic treatment may not have direct effect on honey bee gut community, the gut microbiota dysbiosis caused by high dosage of antibiotic treatment has a cascade effect on the gut community of the nestmates in honeybee colonies.

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“…Previous documentations showed that microsporidian infection significantly increased the mortality of both A. mellifera and A. cerana workers [7,17]. Paris et al [16] assessed the survival rate and eating behavior of western bee workers infected by N. ceranae for 1–22 days, and found that the survival rate of infected workers was significantly lower than that of un-infected workers.…”

Section: Discussionmentioning

confidence: 99%

Impact of Nosema ceranae invasion on sucrose solution consumption, midgut epithelial cell structure, and lifespan of Apis cerana cerana workers

Long

Sun

Fan

et al. 2022

Preprint

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Nosema ceranae is an intracellular fungal parasite for honeybees, leading to chronic disease named bee nosemosis with worldwide distribution. Asian honeybee (Apis cerana) is the original host for N. ceranae, but the impact of N. ceranae infection on A. cerana physiology is largely unknown. In this current work, workers of Apis cerana cerana, a subspecies of Asian honeybee, were artificially inoculated with N. ceranae spores and reared under lab conditions, followed by detection of fungal spore load as well as host sucrose solution consumption, midgut epithelial cell structure, and lifespan. The result of spore counting suggested that the spore load in the host midgut decreased significantly during 1 dpi-2 dpi, whereas that displayed an elevated trend among 2 dpi-13 dpi. The sucrose solution consumption of workers in N. ceranae-inoculated groups among 1 dpi-20 dpi was always higher than that of workers in un-inoculated groups; additionally, the difference of sucrose solution consumption between these two groups at 4 dpi, 5 dpi, and 13 dpi was of significance. Based on microscopic observation of paraffin sections, darkly stained parasites were clearly detected in the midgut epithelial cells of N. ceranae-inoculated workers at 7 dpi-10 dpi, whereas no parasite was observed in those of un-inoculated workers. In addition, the boundaries of un-inoculated host epithelial cells were intact and the darkly stained nucleus were clear, while the boundaries of midgut epithelial cells of N. ceranae-inoculated workers were blurred, the nucleus were almost disappeared, and the nucleic acid substances were diffused. Moreover, the survival rates of workers in both N. ceranae-inoculated groups and un-inoculated groups at 1 dpi-5 dpi were pretty high and then started to decrease at 5 dpi; the survival rate of workers in N. ceranae-inoculated groups was always lower than that in un-inoculated groups, with significant difference between these two groups during 11 dpi-20 dpi. These results together indicate that the quantity of fungal spores continuously elevated with the microsporidian multiplication, causing energetic stress for workers and host cell structure damage, which further negatively affected the host lifespan. Our findings offer a solid basis not only for exploring the molecular mechanism underlying N. ceranae infection but also for investigating the interaction between N. ceranae and eastern honeybee.

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Apis ceranagut microbiota contribute to host health though stimulating host immune system and strengthening host resistance toNosema ceranae

Cited by 28 publications

References 47 publications

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

The Pass-on Effect of Tetracycline-Induced Honey Bee (Apis mellifera) Gut Community Dysbiosis

Impact of Nosema ceranae invasion on sucrose solution consumption, midgut epithelial cell structure, and lifespan of Apis cerana cerana workers

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