Research Article: Habitat-specific variation in gut microbial communities and pathogen prevalence in bumblebee queens (Bombus terrestris)

Date Published: October 25, 2018

Publisher: Public Library of Science

Author(s): L. Bosmans, M. I. Pozo, C. Verreth, S. Crauwels, L. Wilberts, I. S. Sobhy, F. Wäckers, H. Jacquemyn, B. Lievens, James C. Nieh.

http://doi.org/10.1371/journal.pone.0204612

Abstract

Gut microbial communities are critical for the health of many insect species. However, little is known about how gut microbial communities respond to anthropogenic changes and how such changes affect host-pathogen interactions. In this study, we used deep sequencing to investigate and compare the composition of gut microbial communities within the midgut and ileum (both bacteria and fungi) in Bombus terrestris queens collected from natural (forest) and urbanized habitats. Additionally, we investigated whether the variation in gut microbial communities under each habitat affected the prevalence of two important bumblebee pathogens that have recently been associated with Bombus declines (Crithidia bombi and Nosema bombi). Microbial community composition differed strongly among habitat types, both for fungi and bacteria. Fungi were almost exclusively associated with bumblebee queens from the forest habitats, and were not commonly detected in bumblebee queens from the urban sites. Further, gut bacterial communities of urban B. terrestris specimens were strongly dominated by bee-specific core bacteria like Snodgrassella (Betaproteobacteria) and Gilliamella (Gammaproteobacteria), whereas specimens from the forest sites contained a huge fraction of environmental bacteria. Pathogen infection was very low in urban populations and infection by Nosema was only observed in specimens collected from forest habitats. No significant relationship was found between pathogen prevalence and microbial gut diversity. However, there was a significant and negative relationship between prevalence of Nosema and relative abundance of the core resident Snodgrassella, supporting its role in pathogen defense. Overall, our results indicate that land-use change may lead to different microbial gut communities in bumblebees, which may have implications for bumblebee health, survival and overall fitness.

Partial Text

Insects represent one of the most species-rich animal groups on Earth [1, 2] and play an important role in ecosystem functioning [3]. Insects provide numerous important ecosystem services such as pollination, crop protection and detrivory, nutrient cycling, and providing a food source for higher trophic levels [4, 5]. Recent studies have suggested that insects are drastically declining worldwide [6], particularly pollinators [7]. Habitat loss and fragmentation, decline in food resources and nest availability, and increased use of pesticides, as well as climate change have been proposed as the most important factors leading to insect decline [8]. Recently, increased prevalence of diseases and parasites has been suggested to contribute to pollinator decline as well [9]. However, there is increasing consensus that there is likely no single factor that can explain this severe decline, but rather a complex interaction of many factors that act together [8].

Knowledge about the health of bees and bumblebees is important as they are among the most important pollinators for many native plants as well as several crops [42, 43]. Wild bee and bumblebee populations have been in a steady decline worldwide [7], and among several factors, land-use change and increased pathogen prevalence have been proposed to contribute to bee decline [8, 9, 44]. As anthropogenic use of land is likely to increase, we investigated the impact of urbanization on the gut microbial community composition of wild B. terrestris queens, and investigated whether relationships could be established with pathogen infection.

Overall, we observed a striking difference between the gut communities within the midgut and ileum of B. terrestris queens living in urban environments compared to those in forest environments, both for fungi and bacteria. Furthermore, our study provides evidence that the core resident Snodgrassella may have a protective effect against pathogens, and suggests that pathogens may be more prevalent in specimens from natural environments, which may be contradictory to the general assumption of a forest as a source of “pristine”, healthy specimens. Further research with more locations, however, is needed to draw strong conclusions regarding the effect of urbanization on the structure of bumblebee gut commities and bumblebee health and fitness. Possible factors include: landscape structure, pesticide exposure, quantity/ quality and connectivity of food sources, exposure to other arthropod fauna, and other symbiont or pathogen transmission routes. Furthermore, it remains to be investigated whether the same trends will be observed when the rectum is taken into account. Also, additional research using microbial isolates is needed to unravel the precise function of the environmental opportunistic microbes found, and to assess their role in bee health and overall bee fitness.

 

Source:

http://doi.org/10.1371/journal.pone.0204612

 

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