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(Gammaproteobacteria) in Bombus Terrestris Bumblebees

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(Gammaproteobacteria) in Bombus Terrestris Bumblebees Plasticity in the gut microbial community and uptake of Enterobacteriaceae (Gammaproteobacteria) in Bombus terrestris bumblebees’ nests when reared indoors and moved to an outdoor environment Laurian Parmentier, Ivan Meeus, Hadi Mosallanejad, Dirk C. de Graaf, Guy Smagghe To cite this version: Laurian Parmentier, Ivan Meeus, Hadi Mosallanejad, Dirk C. de Graaf, Guy Smagghe. Plasticity in the gut microbial community and uptake of Enterobacteriaceae (Gammaproteobacteria) in Bombus terrestris bumblebees’ nests when reared indoors and moved to an outdoor environment. Apidologie, Springer Verlag, 2016, 47 (2), pp.237-250. 10.1007/s13592-015-0393-7. hal-01532299 HAL Id: hal-01532299 https://hal.archives-ouvertes.fr/hal-01532299 Submitted on 2 Jun 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2016) 47:237–250 Original article * INRA, DIB and Springer-Verlag France, 2015 DOI: 10.1007/s13592-015-0393-7 Plasticity in the gut microbial community and uptake of Enterobacteriaceae (Gammaproteobacteria) in Bombus terrestris bumblebees’ nestswhenrearedindoors and moved to an outdoor environment 1 1 1 2 Laurian PARMENTIER , Ivan MEEUS , Hadi MOSALLANEJAD , Dirk C. de GRAAF , 1 Guy SMAGGHE 1Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, Ghent 9000, Belgium 2Laboratory of Molecular Entomology and Bee Pathology, Faculty of Sciences, Ghent University, Ghent 9000, Belgium Received 7 April 2015 – Revised 8 August 2015 – Accepted 15 September 2015 Abstract – Bombus nests consisting of one queen, brood, and worker adults, are produced indoors for biological pollination in agriculture. In this study, we investigated the gut microbial community in workers of Bombus terrestris when the environment is stable (indoors) or variable (outdoors). When nests were reared indoors under standardized conditions, we identified a small gut microbial community consisting of Neisseriaceae , Orbaceae , Lactobacillaceae ,andBifidobacteriaceae , and the age of bumblebee nests and workers did not affect the alpha and beta diversity, confirming a stable microbiota. Secondly, when indoor-reared nests were moved to outdoors, we observed a major shift in the microbial community, especially in the newborn workers fully developed in the outdoor conditions, with a significant colonization of Enterobacteriaceae . Our new findings are discussed in relation to host- associated core and non-core bacteria in bumblebees including possible implications for host functioning. Bombus terrestris / generalist pollinator / microbiota / plasticity / Enterobacteriaceae / reared bumblebees 1. INTRODUCTION communities of specific bacteria, which is especially true in social insects (Engel and Moran 2013). Insects easily outnumber other animal clades in Within the clade of social bees, research on micro- the world inhabiting a diverse range of ecosystems. bial communities has been focusing on honeybees Insects are, in many cases, dependent on functions (Martinson et al. 2012; Moran et al. 2012)and provided by bacterial symbionts (Brownlie and bumblebees (Koch and Schmid-Hempel 2011b; Johnson 2009;Bassetetal.2012), including gut Koch et al. 2012; Meeus et al. 2013;Lietal. microbiota with beneficial functions in nutrition 2015; Praet et al. 2015) because of their important (Salem et al; 2012) and protection (Dillon and pollinating role in natural ecosystems and of many Charnley 1986, 1988). Some insects harbor gut agricultural crops, together with a growing evidence of their dramatic declines worldwide (Ghazoul Electronic supplementary material The online version of 2005;Lebuhnetal.2013). this article (doi:10.1007/s13592-015-0393-7) contains The social nesting behavior of honeybees and supplementary material, which is available to authorized bumblebees enables the transfer of gut bacteria users. over the generations, allowing a close association Corresponding author: G. Smagghe, with the host (Powell et al. 2014). Indeed, social [email protected] bees, as opposed to solitary bees, generally harbor Manuscript editor: David Tarpy host-associated bacterial groups, defined as Bcore 238 L. Parmentier et al. set,^ and the latter are generally found in the gut Westerlo, Belgium). All colonies contained one microbiota of social bees (Kaltenpoth 2011;Koch queen, new queen brood but without adult and Schmid-Hempel 2011b; Cariveau et al. 2014). workers. The nests were kept in the lab at standard Core bacteria dominating the gut of social honey- conditions of 28–30 °C and 60–65 % relative bees and bumblebees have been implicated in ben- humidity and continuous darkness, and they were eficial functions such as digestion and protection fed ad libitum with artificial nectar (Biogluc®, (Klungness and Peng 1984;Forsgrenetal.2010; Biobest) and pollen clumps (Soc. Coop. Koch et al. 2012; Vásquez et al. 2012; Kwong et al. Apihurdes, Pinofranqueado-Caceres, Spain) as 2014). Multiple conditions have been reported energy and protein sources, respectively influencing the bacterial gut community, including (Mommaerts et al. 2006). For the six bumblebee the environment, host age, habitat, pathogens, and nests, we labeled the queen and then also each diet (Dillon et al. 2010; Evans and Schwarz 2011; newborn worker adult on a daily basis with a Hu et al. 2014;Yunetal.2014). unique marking disc (Bijenhof, Bissegem, Bel- Currently, the buff-tailed bumblebee Bombus gium) to the dorsal thorax. The six nests were terrestris is reared indoors for the biological polli- used for two experiments where in the first exper- nation in agriculture. This species is widely distrib- iment, three nests were kept indoors under the uted and native to Europe, coastal North Africa, standard conditions as described earlier, while in and West and Central Asia (Goulson 2010). Due to the second experiment, the other three nests were the decline of bees worldwide, research has been moved outdoors. The experiments were carried focusedondiseases(Fürstetal.2014) and patho- out between end August up to end September gen spillover (Meeus et al. 2011). Besides, there and early October 2012. has been little research on the gut microbial com- munity and the dynamics of indoor-reared bumble- 2.2. Experiment 1: bumblebee nests kept bees foraging in an environment outdoors. under standard conditions indoors In this paper, we used 16S rRNA Illumina deep sequencing to identify the gut microbial communi- Three nests were followed for 60 days during ty in workers of B. terrestris from indoor-reared the rearing period in the lab under standard con- nests. In a first experiment, we determined the ditions. We aimed to investigate the impact of age growth and richness of this microbial community of the nest and the individual bumblebee worker when the nests were kept under indoor conditions. in the nest. Therefore, we defined two age periods Our ambitions were to determine the dominant of the nest: young nest (Yn; 4- to 11-day old nest) bacteria in indoor-reared nests and the stability of and old nest (On; 40- to 46-day old nest) and two these bacteria in function of the age of the adults age periods of the workers: young bee (Yb;4to and the nest. In a second experiment, the indoor- 10 days old) and old bee (Ob;28to35daysold). reared bumblebee nests were moved to outdoors to When combining the age period of the nest with investigate the plasticity of the gut microbial com- the age of the individual workers, we defined munity in the workers of different ages. In summa- three test groups: young nest, young bee (YnYb); ry, the new data found in this study are of use to old nest, old bee (OnOb); and old nest, young bee discuss the relationship between core and non-core (OnYb). In total, we sampled eight workers per bacteria in bumblebees and to generate new in- test group. Sampled bumblebees were stored in- sights in the gut microbial stability of indoor- dividually at −70 °C until dissection of the gut. reared bumblebee hives when moved to outdoors. 2.3. Experiment 2: indoor-reared 2. MATERIAL AND METHODS bumblebee nests moved to an outdoor environment 2.1. Bumblebee nests and insect labeling In parallel to experiment 1, we kept the three Six nests of B. terrestris were obtained from a other nests indoors in the lab so that they devel- bumblebee mass-rearing facility (Biobest, oped an initial indoor-reared microbiota. When Plasticity in reared B. terrestris nests moved to outdoors 239 placed outdoors, the three nests developed further selected foraging workers (foragers) that had at under natural conditions during 50 days. The out- least five flights per day under good weather doors study site (51° 01 32.57 N; 3° 42 46.10 conditions (excluding rainy days and tempera- O) was located in a residential area in the city of tures <15 °C). Ghent (Belgium) with landscape metrics of an urbanized environment (Parmentier et al. 2014). 2.4. Gut samples processing, Illumina As shown in Figure S1, each nest was placed in a sequencing, and identification separate polystyrene-box (25×35×25 cm) with the entrance directed to the east and further treated as The gut, including the crop, was dissected from described in Parmentier et al. (2014). the different bumblebee workers and transferred In the outdoors experiment, we defined three individually into a 1.5-mL Eppendorf tube. All age periods of the nests: young nest (Yn,4-to11- equipment used was disinfected with 75 % etha- day old nest); middle-aged nest (Mn, 28- to 34- nol between each individual dissection. The ex- day old nest); and old nest (On, 40- to 46-day old traction of bacterial DNA was done as previously nest), and three age periods of the workers: young described (Meeus et al.
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