Honey bees as models for gut microbiota research

Zheng, Hao; Steele, Margaret I.; Leonard, Sean P.; Motta, Erick V. S.; Moran, Nancy A.

doi:10.1038/s41684-018-0173-x

Cited by 207 publications

(212 citation statements)

References 140 publications

Supporting

Mentioning

204

Contrasting

Unclassified

Order By: Relevance

“…Within the bee-associated Lactobacilli, Lactobacillus mellifera and L. mellis form a distinct phylogenetic cluster referred as Lactobacillus Firm-4, and the species Lactobacillus apis, L helsingborgensis, L. kimbladii, L. kullabergensis, and L. melliventris are referred as Lactobacillus Firm-5 [49]. Both clusters are located within the hindgut, Lactobacillus Firm-4 in the rectum, L. Firm-5 in the ileum and rectum [49,50]. While these two clusters are rarely detected outside the hindgut, Lactobacillus kunkeei is also found outside the honey bee body in the hive.…”

Section: Discussionmentioning

confidence: 99%

The trisaccharide melezitose impacts honey bees and their intestinal microbiota

et al. 2020

View full text Add to dashboard Cite

In general, honey bees (Apis mellifera L.) feed on honey produced from collected nectar. In the absence of nectar, during certain times of the year or in monocultural landscapes, honey bees forage on honeydew. Honeydew is excreted by different herbivores of the order Hemiptera that consume phloem sap of plant species. In comparison to nectar, honeydew is composed of a higher variety of sugars and additional sugars with higher molecular weight, like the trisaccharide melezitose that can be a major constituent of honeydew. However, melezitose-containing honey is known to cause malnutrition in overwintering honey bees. Following the hypothesis that melezitose may be the cause for the so called 'honeydew flow disease', three independent feeding experiments with caged bees were conducted in consecutive years. Bees fed with melezitose showed increased food uptake, higher gut weights and elevated mortality compared to bees fed a control diet. Moreover, severe disease symptoms, such as swollen abdomen, abdomen tipping and impaired movement were observed in melezitose-fed bees. 16S-amplicon sequencing indicated that the melezitose diet changed the species composition of the lactic acid bacteria community within the gut microbiota. Based on these results, we conclude that melezitose cannot be easily digested by the host and may accumulate in the hindgut. Within cages or during winter, when there is no opportunity for excretion, the accumulated melezitose can cause severe intestinal symptoms and death of the bees, probably as result of poor melezitose metabolism capabilities in the intestinal microbiota. These findings confirm the causal relation between the trisaccharide melezitose and the honeydew flow disease and indicate a possible mechanism of pathogenesis. OPEN ACCESSCitation: Seeburger VC, D'Alvise P, Shaaban B, Schweikert K, Lohaus G, Schroeder A, et al. (2020) The trisaccharide melezitose impacts honey bees and their intestinal microbiota. PLoS ONE 15(4): e0230871. https://doi.org/10. Data Availability Statement:The 16S amplicon sequence data generated during the current study are available from Dryad using the doi: https://doi. org/10.5061/dryad.3ffbg79f8. symptoms of this food toxicosis are diverse: a high number of bees remain at the hive entrance instead of foraging, bees experience massive loss of hair (which may indicate complication with virus infections) and changes their behavioural patterns [3]. Even necrotic appearances could be shown in the midgut of honey bees when fed with honeydew honey in tent experiments [3]. This condition can deteriorate to a point where colonies collapse within short time. This is known to beekeepers and discussed in beekeeping journals [4], but the precise reason has remained unknown.Honey bees primarily forage on nectar. The three most common nectar sugars are the two monosaccharides glucose and fructose, and the disaccharide sucrose [5]. However, seasonally or locally nectar plants are lacking, and nectar is not available. In such situations honey bees tend to forage on honey...

show abstract

Section: Discussionmentioning

confidence: 99%

The trisaccharide melezitose impacts honey bees and their intestinal microbiota

et al. 2020

View full text Add to dashboard Cite

show abstract

“…In social insects, such as honey bees, intestinal bacteria are transmitted and shared by colony members through oral–faecal transmission, oral trophallactic interaction, consumption of stored pollen or beebread, interactions with older bees within the hive and contact with hive material during the adult phase [ 3 , 4 ]. With its simple and characteristic composition, the honey bee gut microbiota provides an excellent model for studying the functional and structural aspects of the bacterial communities associated with the gut [ 5 , 6 , 7 ].…”

Section: Introductionmentioning

confidence: 99%

Inter- and Intra-Species Diversity of Lactic Acid Bacteria in Apis mellifera ligustica Colonies

et al. 2020

View full text Add to dashboard Cite

Lactic acid bacteria could positively affect the health of honey bees, including nutritional supplementation, immune system development and pathogen colonization resistance. Based on these considerations the present study evaluated predominant Lactic Acid Bacteria (LAB) species from beebread as well as from the social stomach and midgut of Apis mellifera ligustica honey bee foragers. In detail, for each compartment, the diversity in species and biotypes was ascertained through multiple culture-dependent approaches, consisting of Polymerase Chain Reaction-Denaturing Gradient Gel Electrophoresis (PCR-DGGE), 16S rRNA gene sequencing and Randomly Amplified Polymorphic DNA-Polymerase Chain Reaction (RAPD-PCR). The study of a lactic acid bacteria community, performed with PCR-DGGE and sequence analysis targeting the V1–V3 region of the 16S rRNA gene (rDNA), highlighted the presence of a few species, including Apilactobacillus kunkeei, Lactiplantibacillus plantarum, Fructobacillus fructosus, Levilactobacillus brevis and Lactobacillus delbrueckii subsp. lactis. Depending on the different compartments, diverse levels of biodiversity in species were found. Particularly, a very low inter-species biodiversity was detected in the midgut that was prevalently dominated by the presence of Apilactobacillus kunkeei. On the other hand, the beebread was characterized by a reasonable biodiversity showing the presence of five species and the predominance of Apilactobacillus kunkeei, Lactiplantibacillus plantarum and Fructobacillus fructosus. The RAPD-PCR analysis performed on the three predominant species allowed the differentiation into several biotypes for each species. Moreover, a relationship between biotypes and compartments has been detected and each biotype was able to express a specific biochemical profile. The biotypes that populated the social stomach and midgut were able to metabolize sugars considered toxic for bees while those isolated from beebread could contribute to release useful compounds with functional properties. Based on this knowledge, new biotechnological approaches could be developed to improve the health of honey bees and the quality of bee products.

show abstract

“…Although stable relative to larvae, dominant butterfly-associated microbes do exhibit higher levels of interindividual variability as compared with obligate nutritional endosymbionts or gut microbes of some other insect groups. For example, in honey bees, >98% of sequences belong to a honey bee-specific set of 5-9 bacterial species (57). We found that ~80-90% of sequences in a given butterfly species' microbiome belonged to a set of 10 core bacterial genera.…”

Section: Discussionmentioning

confidence: 75%

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

Hammer

Dickerson

McMillan

et al. 2019

Preprint

View full text Add to dashboard Cite

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...

show abstract

Honey bees as models for gut microbiota research

Cited by 207 publications

References 140 publications

The trisaccharide melezitose impacts honey bees and their intestinal microbiota

The trisaccharide melezitose impacts honey bees and their intestinal microbiota

Inter- and Intra-Species Diversity of Lactic Acid Bacteria in Apis mellifera ligustica Colonies

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

Contact Info

Product

Resources

About