Abstract

Simple SummaryA vast array of microorganisms colonize invertebrates and vertebrates. Most of these microbes reside in the digestive tract, where they constitute the intestinal (gut) microbiome. Some microbes are commensal, coexisting with their host without causing harm, while others can be mutualistic or pathogenic. Mutualistic microorganisms perform many health-related functions such as promoting digestion and acquisition of nutrients; hormone regulation; maintenance and control of the immune system; regulation of homeostasis and stress physiology of the body; insecticide resistance; production of certain vitamins; and providing protection against pathogenic microorganisms, parasites, and diseases. Bee-specific bacterial genera such as Lactobacillus, Snodgrassella, and Gilliamella dominate the gut communities of many bumblebees. This study confirmed Lactobacillus, Snodgrassella, and Gilliamella as dominant gut bacteria of the buff-tailed bumblebee Bombus terrestris in the agricultural landscape. However, we show that the guts of B. terrestris from natural forest habitats can be dominated by fructose-associated Fructobacillus spp. Our findings may have important implications for understanding the ecological role of bumblebees and the reasons for the decline of key pollinators.Bumblebees are key pollinators in agricultural landscapes. However, little is known about how gut microbial communities respond to anthropogenic changes. We used commercially produced colonies of buff-tailed bumblebees (Bombus terrestris) placed in three habitats. Whole guts (midgut, hindgut, and rectum) of B. terrestris specimens were dissected from the body and analyzed using 16S phylogenetic community analysis. We observed significantly different bacterial community composition between the agricultural landscapes (apple orchards and oilseed rape (Brassica napus) fields) and forest meadows, whereas differences in gut communities between the orchards and oilseed rape fields were nonsignificant. Bee-specific bacterial genera such as Lactobacillus, Snodgrassella, and Gilliamella dominated gut communities of B. terrestris specimens. In contrast, the guts of B. terrestris from forest meadows were dominated by fructose-associated Fructobacillus spp. Bacterial communities of workers were the most diverse. At the same time, those of males and young queens were less diverse, possibly reflecting greater exposure to the colony’s inner environment compared to the environment outside the colony, as well as bumblebee age. Our results suggest that habitat quality, exposure to environmental microbes, nectar quality and accessibility, and land use significantly affect gut bacterial composition in B. terrestris.

Highlights

  • Illumina MiSeq sequencing of the bacterial 16S rRNA amplicons from different habitats and bumblebee castes yielded a total of 15,983,683 raw reads

  • The total numbers of bacterial OTUs in the samples collected in apple orchards, oilseed rape fields, and forest meadows were 13,836, 12,210, and 4705, respectively

  • Our results showed dominance of Lactobacillus spp. and Snodgrassella spp. in the guts of bees collected from both apple orchards and oilseed rape fields

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Summary

Introduction

Microorganisms have a significant influence on their hosts’ behavioral responses, reproductive output, and development [1,2], and compositional changes in the microbiome have important consequences on host activity and fitness [3,4]. The diversity, stability, and composition of microbial communities in the gut are affected by a number of factors such as habitat, season, host density, intensity of intraspecific and interspecific competition, diet, exposure to agrochemicals and antimicrobials, and interactions between populations of the gut microbial community [2–5] Studies on these factors and their interactions need more attention in order for us to further understand the role of the microbiome. Pollination is critical for sustainable food production in human-managed ecosystems, as most flowering plant species only produce seeds if animal pollinators visit their flowers and provide pollination services [8] Pollinators such as insects, birds, and bats affect almost 40% of global crop production [9]

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