Microbiome assembly and maintenance across the lifespan of bumble bee workers

Hammer, Tobin J.; Easton‐Calabria, August; Moran, Nancy A.

doi:10.1111/mec.16769

Cited by 20 publications

(23 citation statements)

References 199 publications

(299 reference statements)

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“…(2023a) reported a community shift of the bumble bee microbiota with age, resulting in a decrease in Schmidhempelia and the establishment of Gilliamella , while proportions of Lactobacillus remain relatively stable over a period of 60 days. Though Schmidhempelia has been described as dominant member of the microbiota of the common eastern bumble bee ( B. impatiens ) (Hammer et al, 2023a), we found it only with low abundances within a few individuals of B. terrestris . We observed also larger shifts in community composition, but a decrease in relative abundance of Gilliamella , while Lactobacillaceae were increasing within a 35 day period.…”

Section: Discussioncontrasting

confidence: 68%

“…Upon hatching, adult bumble bees, much like honeybees, emerge bacteria-free and acquire their microbiota from their food, hive environment or nestmates (Koch and Schmid-Hempel, 2011b; Hammer et al, 2021b). This process happens within the first 4 days of the adult life so that the overall microbial load remains relatively stable with progressing adult age for B. impatiens (Hammer et al, 2023a). When reared indoors, the microbiota of B. terrestris and B. impatiens shows no larger change in alpha diversity over time (Parmentier et al, 2016; Hammer et al, 2023a).…”

Section: Discussionmentioning

confidence: 99%

“…This process happens within the first 4 days of the adult life so that the overall microbial load remains relatively stable with progressing adult age for B. impatiens (Hammer et al, 2023a). When reared indoors, the microbiota of B. terrestris and B. impatiens shows no larger change in alpha diversity over time (Parmentier et al, 2016; Hammer et al, 2023a). This was clearly different in our setup, as the placement into outdoor environments resulted in diversification of bumble bee microbiota, observable by an increase in in alpha diversity as well as an increase in sample dissimilarity over time.…”

Section: Discussionmentioning

confidence: 99%

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Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

Weinhold,

Grüner,

Keller

2023

Preprint

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QuestionThe large earth bumble bee (Bombus terrestris) maintains a social core gut-microbiota, similar as known from the honey bee, which plays an important role for host health and resistance. Experiments under laboratory conditions with commercial hives are limited to these vertically transmitted microbes and neglect variability by environmental influences and external acquisition of microbes. Various environmental and landscape-level factors may have an impact on the gut-microbiota of pollinating insects, with consequences for pollinator health and fitness in agroecosystems. Still, it is not fully clear whether access to a higher vs lower flower diversity will have a significant influence on the bumble bee microbiota. Here, we tested in a semi-field experiment how strongly the bumble bee microbiota changes over time when exposed to different flower diversities within outdoor flight cages. We used commercial hives to distinguish between vertically and horizontally transmitted bacteria, respectively from the nest environment or the exposed outside environment.ResultThe sequential sampling of foraging workers over a period of 35 days indicated a temporal progression of the bumble bee microbiota when exposed to outside conditions. The microbiota became not only more diverse, but changed in composition and variability over time. We observed a major increase in relative abundance of the familiesLactobacillaceae,BifidobacteriaceaeandWeeksellaceae. In contrast, major core taxa likeSnodgrassellaandGilliamelladeclined in their relative abundance over time. The genusLactobacillusshowed a high diversity and strain specific turnover, so that only specific ASVs showed an increase over time, while others had a more erratic occurrence pattern. Exposure to different flower diversities had no significant influence on the bumble bee microbiota.ConclusionThe bumble bee microbiota showed a dynamic temporal progression with distinct compositional changes and diversification over time. The exposure of bumble bees to environmental conditions, or environmental microbes, increases dissimilarity and changes the gut-community composition compared to laboratory rearing conditions. This shows the importance of environmental influences on the temporal dynamic and progression of the bumble bee microbiota.Scope statementBumble bees (Bombus terrestris) are, next to the honey bee, commercially important pollinators and widely used to enhance crop pollination service within greenhouse environments. They host a similar, but characteristic, set of core-microbiota which are of known importance for bumble bee health. Despite this, bumble bees harbor their own specific set of symbionts, which do not occur within the honey bee and seem to be more easily influenced by colonization of environmental microbes. While experiments under controlled lab-based rearing conditions often lack the influence of environmental or landscape-level drivers, field-based observation can often not resolve the influence of a single factor. One major unresolved question is which environmental factor influences the microbiota of social pollinators by environmental microbes. Especially whether monocultures (low flower diversity) areper serather detrimental to microbiota composition compared to more balanced and diverse pollen provisions (high flower diversity). Within this article, we investigated the influence of different flower diversities as potential drivers of the bumble bee gut-microbiota under semi-field conditions. We used outdoor cages which contained a flower diversity gradient to specifically test how a low and high diversity of flower resources could influence the bumble bee microbiota over time.

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Section: Discussioncontrasting

confidence: 68%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

Weinhold,

Grüner,

Keller

2023

Preprint

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“…Given we used standard rearing methods and diet, we hypothesize that lower bacterial titer may be due to the age of bees we sampled. Previous work in bumble bees shows that bacterial density increases with worker age, saturating approximately four days after worker emergence 73 . Future work could examine how phage abundance and composition changes through worker development and if this reflects previous observations of bacterial succession with worker age 17 .…”

Section: Discussionmentioning

confidence: 94%

Targeted Viromes and Total Metagenomes Capture Distinct Components of Bee Gut Phage Communities

Sbardellati,

Vannette

2024

Preprint

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Despite being among the most abundant biological entities on earth, bacteriophage (phage) remain an understudied component of host-associated systems. One limitation to studying host-associated phage is the lack of consensus on methods for sampling phage communities. Here, we compare paired total metagenomes and viral size fraction metagenomes (viromes) as methods for investigating the dsDNA viral communities associated with the GI tract of two bee species: the European honey bee Apis mellifera and the eastern bumble bee Bombus impatiens. We find that viromes successfully enriched for phage, thereby increasing phage recovery, but only in honey bees. In contrast, for bumble bees, total metagenomes recovered greater phage diversity. Across both bee species, viromes better sampled low abundance and low occupancy phage, while total metagenomes were biased towards sampling temperate phage and the most prominent phage. Additionally, many of the phage captured by total metagenomes were absent altogether from viromes. Comparing between bees, we show that phage communities in commercially reared bumble bees are significantly reduced in diversity compared to honey bees, likely reflecting differences in bacterial titer and diversity. In a broader context, these results highlight the complementary nature of total metagenomes and targeted viromes, especially when applied to host-associated environments. Overall, we suggest that studies interested in assessing total communities of host-associated phage should consider using both approaches. However, given the constraints of virome sampling, total metagenomes may serve to sample phage communities with the understanding that they will preferentially sample dominant and temperate phage.

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“…Our quantification of Stammera titers in adults focused on young, reproductively active beetles (Figure 5). How senescence and diapause impact symbiont density is also of interest and worthy of exploring in future studies [65][66][67]72]. Tortoise beetles experimentally induced to enter diapause cease feeding and pause egg-laying [70].…”

Section: Stammera Population Dynamics Relative To Adult Nutritional A...mentioning

confidence: 99%

Extracellular symbiont colonizes insect during embryo development

Porras,

Pons,

García-Lozano

et al. 2023

Preprint

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Insects typically acquire their beneficial microbes early in development. Endosymbionts housed intracellularly are commonly integrated during oogenesis or embryogenesis, whereas extracellular microbes are only known to be acquired after hatching by immature instars such as larvae or nymphs. Here, however, we report on an extracellular symbiont that colonises its host during embryo development. Tortoise leaf beetles (Chrysomelidae: Cassidinae) host their digestive bacterial symbiontStammeraextracellularly within foregut symbiotic organs, and in ovary-associated glands to ensure its vertical transmission. We outline the initial stages of symbiont colonization and observe that while the foregut symbiotic organs develop three days prior to larval emergence, they remain empty until the final 24 hours of embryo development. Infection byStammeraoccurs during that timeframe, and prior to hatching. By experimentally manipulating symbiont availability to embryos in the egg, we describe a 12-hour developmental window governing colonization byStammera. Symbiotic organs form normally in aposymbiotic larvae, demonstrating that theseStammera-bearing structures develop autonomously. In adults, the foregut symbiotic organs are already colonized following metamorphosis and host a stableStammerapopulation to facilitate folivory. The ovary-associated glands, however, initially lackStammera. Symbiont abundance subsequently increases within these transmission organs, thereby ensuring sufficient titers at the onset of oviposition ∼29 days following metamorphosis. Collectively, our findings reveal thatStammeracolonization precedes larval emergence, where its proliferation is eventually decoupled in adult beetles to match the nutritional and reproductive requirements of its host.

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Microbiome assembly and maintenance across the lifespan of bumble bee workers

Cited by 20 publications

References 199 publications

Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

Targeted Viromes and Total Metagenomes Capture Distinct Components of Bee Gut Phage Communities

Extracellular symbiont colonizes insect during embryo development

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