Gut microbiota affects development and olfactory behavior in Drosophila melanogaster

被引:92
作者
Qiao, Huili [1 ,2 ]
Keesey, Ian W. [1 ]
Hansson, Bill S. [1 ]
Knaden, Markus [1 ]
机构
[1] Max Planck Inst Chem Ecol, Dept Evolutionary Neuroethol, D-07745 Jena, Germany
[2] Nanyang Normal Univ, Henan Prov Key Lab Funiu Mt Insect Biol, Nanyang 473061, Peoples R China
关键词
Host-microbe interaction; Olfaction; Gut bacteria; Yeast; Behavior; OVIPOSITION PREFERENCE; MALE COURTSHIP; ATTRACTION; PHEROMONE; RECEPTOR; HOMEOSTASIS; NEURONS; ODORS;
D O I
10.1242/jeb.192500
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
It has been shown that gut microbes are very important for the behavior and development of Drosophila, as the beneficial microbes are involved in the identification of suitable feeding and egg-laying locations. However, in what way these associated gut microbes influence the fitness-related behaviors of Drosophila melanogaster remains unclear. Here, we show that D. melanogaster exhibits different behavioral preferences towards gut microbes. Both adults and larvae were attracted by the volatile compounds of Saccharomyces cerevisiae and Lactobacillus plantarum, but were repelled by Acetobacter malorum in behavioral assays, indicating that an olfactory mechanism is involved in these preference behaviors. While the attraction to yeast was governed by olfactory sensory neurons expressing the odorant co-receptor Orco, the observed behaviors towards the other microbes were retained in flies lacking this co-receptor. By experimentally manipulating the microbiota of the flies, we found that flies did not strive for a diverse microbiome by increasing their preference towards gut microbes that they had not experienced previously. Instead, in some cases, the flies even increased preference for the microbes on which they were reared. Furthermore, exposing Drosophila larvae to all three microbes promoted Drosophila development, while exposure to only S. cerevisiae and A. malorum resulted in the development of larger ovaries and in increased egg numbers in an oviposition assay. Thus, our study provides a better understanding of how gut microbes affect insect behavior and development, and offers an ecological rationale for preferences of flies for different microbes in their natural environment.
引用
收藏
页数:10
相关论文
共 48 条
[1]   Acid sensing by the Drosophila olfactory system [J].
Ai, Minrong ;
Min, Soohong ;
Grosjean, Yael ;
Leblanc, Charlotte ;
Bell, Rati ;
Benton, Richard ;
Suh, Greg S. B. .
NATURE, 2010, 468 (7324) :691-U112
[2]   Influence of dietary yeasts on Drosophila melanogaster life-history traits [J].
Anagnostou, Christiana ;
Dorsch, Monika ;
Rohlfs, Marko .
ENTOMOLOGIA EXPERIMENTALIS ET APPLICATA, 2010, 136 (01) :1-11
[3]   CIS-VACCENYL ACETATE AS AN AGGREGATION PHEROMONE IN DROSOPHILA-MELANOGASTER [J].
BARTELT, RJ ;
SCHANER, AM ;
JACKSON, LL .
JOURNAL OF CHEMICAL ECOLOGY, 1985, 11 (12) :1747-1756
[4]   Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development [J].
Becher, Paul G. ;
Flick, Gerhard ;
Rozpedowska, Elzbieta ;
Schmidt, Alexandra ;
Hagman, Arne ;
Lebreton, Sebastien ;
Larsson, Mattias C. ;
Hansson, Bill S. ;
Piskur, Jure ;
Witzgall, Peter ;
Bengtsson, Marie .
FUNCTIONAL ECOLOGY, 2012, 26 (04) :822-828
[5]   Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors [J].
Becher, Paul G. ;
Bengtsson, Marie ;
Hansson, Bill S. ;
Witzgall, Peter .
JOURNAL OF CHEMICAL ECOLOGY, 2010, 36 (06) :599-607
[6]   Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila [J].
Benton, Richard ;
Vannice, Kirsten S. ;
Gomez-Diaz, Carolina ;
Vosshall, Leslie B. .
CELL, 2009, 136 (01) :149-162
[7]   Gut-associated microbes of Drosophila melanogaster [J].
Broderick, Nichole A. ;
Lemaitre, Bruno .
GUT MICROBES, 2012, 3 (04) :307-321
[8]   Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host-Microbe Model System [J].
Chandler, James Angus ;
Lang, Jenna Morgan ;
Bhatnagar, Srijak ;
Eisen, Jonathan A. ;
Kopp, Artyom .
PLOS GENETICS, 2011, 7 (09)
[9]   Ionotropic Receptors Mediate Drosophila Oviposition Preference through Sour Gustatory Receptor Neurons [J].
Chen, Yan ;
Amrein, Hubert .
CURRENT BIOLOGY, 2017, 27 (18) :2741-+
[10]   Distinct Shifts in Microbiota Composition during Drosophila Aging Impair Intestinal Function and Drive Mortality [J].
Clark, Rebecca I. ;
Salazar, Anna ;
Yamada, Ryuichi ;
Fitz-Gibbon, Sorel ;
Morselli, Marco ;
Alcaraz, Jeanette ;
Rana, Anil ;
Rera, Michael ;
Pellegrini, Matteo ;
Ja, William W. ;
Walker, David W. .
CELL REPORTS, 2015, 12 (10) :1656-1667