The gut microbiota of bumblebees

Hammer, Tobin J.; Le, Eli; Martin, A.; Moran, Nancy A.

doi:10.1007/s00040-021-00837-1

Cited by 49 publications

(87 citation statements)

References 134 publications

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“…In a recent study, high sucrose diets resulted in more diverse honeybee midgut communities, while diets high in glucose or fructose led to more diverse hindgut communities [70]. Given that the gut microbiome of social bees can greatly affect their host's health through both metabolization of carbon-rich food sources and modulation of the immune system [71][72][73], greater consideration of links between microbiomes of nectar and the host gut is warranted.…”

Section: (B) Microbially Induced Effects On Pollinator Healthmentioning

confidence: 99%

Potential effects of nectar microbes on pollinator health

Martin

Schaeffer

Fukami

2022

Phil. Trans. R. Soc. B

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Floral nectar is prone to colonization by nectar-adapted yeasts and bacteria via air-, rain-, and animal-mediated dispersal. Upon colonization, microbes can modify nectar chemical constituents that are plant-provisioned or impart their own through secretion of metabolic by-products or antibiotics into the nectar environment. Such modifications can have consequences for pollinator perception of nectar quality, as microbial metabolism can leave a distinct imprint on olfactory and gustatory cues that inform foraging decisions. Furthermore, direct interactions between pollinators and nectar microbes, as well as consumption of modified nectar, have the potential to affect pollinator health both positively and negatively. Here, we discuss and integrate recent findings from research on plant–microbe–pollinator interactions and their consequences for pollinator health. We then explore future avenues of research that could shed light on the myriad ways in which nectar microbes can affect pollinator health, including the taxonomic diversity of vertebrate and invertebrate pollinators that rely on this reward. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

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Section: (B) Microbially Induced Effects On Pollinator Healthmentioning

confidence: 99%

Potential effects of nectar microbes on pollinator health

Martin

Schaeffer

Fukami

2022

Phil. Trans. R. Soc. B

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“…However, as is the case with humans [15,16], the ‘old friends hypothesis’ may be more applicable to understanding insect immunity. A coevolved gut microbiome has been identified in key insect pollinators (honeybees: [25], bumblebees: [26]), and interactions between the insect immune system and the gut microbiome are well-documented [27,28], as are interactions between the gut microbiome and parasites [29], both of which can be viewed as prerequisites for the ‘old friends hypothesis’ to apply. Consequently, microbes may play a key role in the development, maintenance and function of the immune system of insect pollinators and thus have a positive impact on individual health [27].…”

Section: Parasites and Wild Pollinator Health Sensu Strictomentioning

confidence: 99%

Complex networks of parasites and pollinators: moving towards a healthy balance

Brown

2022

Phil. Trans. R. Soc. B

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Parasites are viewed as a major threat to wild pollinator health. While this may be true for epidemics driven by parasite spillover from managed or invasive species, the picture is more complex for endemic parasites. Wild pollinator species host and share a species-rich, generalist parasite community. In contrast to the negative health impacts that these parasites impose on individual hosts, at a community level they may act to reduce competition from common and abundant pollinator species. By providing rare species with space in which to exist, this will act to support and maintain a diverse and thus healthier pollinator community. At this level, and perhaps paraxodically, parasites may be good for pollinators. This stands in clear contrast to the obvious negative impacts of epidemic and spillover parasites on wild pollinator communities. Research into floral resources that control parasites could be best employed to help design landscapes that provide pollinators with the opportunity to moderate their parasite community, rather than attempting to eliminate specific parasites from wild pollinator communities. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

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“…Bumblebees ( Bombus spp.) differ from honeybees in many ways that likely relate to microbiome dynamics (35). Workers exhibit comparatively weak age polyethism (temporal division of labor); tasks are generally carried out by workers of all ages, though some tasks are more likely to be performed at certain ages (52).…”

Section: Introductionmentioning

confidence: 99%

“…Workers exhibit comparatively weak age polyethism (temporal division of labor); tasks are generally carried out by workers of all ages, though some tasks are more likely to be performed at certain ages (52). Symbionts are transmitted between generations by a single queen, instead of by a large group of workers as in honeybees; this changes the bottleneck size, and potentially, selection on caste-specific maintenance processes (35). They also lack certain bacteria characteristic of honeybees and have gained Candidatus Schmidhempelia bombi (hereafter, Schmidhempelia ) (41, 53).…”

Section: Introductionmentioning

confidence: 99%

“…In bumblebees, a solitary queen founds the colony and produces cohorts of (mostly) nonreproductive workers; reproductive offspring (queens and males) are produced toward the end of the colony cycle (64). Given that: i ) age-specific survival probabilities are similar over much of the bumblebee worker lifespan (65, 66), ii ) even old workers contribute to colony reproduction (52), and iii ) there is a need to transmit the core gut symbionts—and not pathogens or parasites—to new queens (35), one may expect only minimal senescence of worker microbiomes, gut physiology, and immunity. Indeed, some aspects of systemic immunity in bumblebees remain stable or increase with age (67).…”

Section: Introductionmentioning

confidence: 99%

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Microbiome assembly and maintenance across the lifespan of bumble bee workers

Hammer

Easton‐Calabria

Moran

2022

Preprint

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How a host’s microbiome changes over its lifespan can influence development and aging. As these temporal patterns have only been described in detail for humans and a handful of other hosts, an important next step is to compare microbiome dynamics across a broader array of host-microbe symbioses, and to investigate how and why they vary. Here we characterize the temporal dynamics and stability of the bumblebee worker gut microbiome. Bumblebees are a useful symbiosis model given their relatively well-understood life history and simple, host-specific gut bacterial communities. Furthermore, microbial dynamics may influence bumblebee health and pollination services. We combined high-temporal-resolution sampling with 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics to characterize gut microbiomes over the adult lifespan of Bombus impatiens workers. To understand how hosts may control (or lose control of) the gut microbiome as they age, we also sequenced hindgut transcriptomes. We found that, at the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. At the same time, partitioning of strain-level bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome—including expression of key immunity genes—stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumblebees, maintenance of both microbiomes and immunity contribute to the inclusive fitness of workers, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession, and for comparative analyses with other host-microbe symbioses.

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The gut microbiota of bumblebees

Cited by 49 publications

References 134 publications

Potential effects of nectar microbes on pollinator health

Potential effects of nectar microbes on pollinator health

Complex networks of parasites and pollinators: moving towards a healthy balance

Microbiome assembly and maintenance across the lifespan of bumble bee workers

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