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Symbiotic roles of the honey bee gut microbiota

English title Symbiotic roles of the honey bee gut microbiota
Applicant Engel Philipp
Number 160345
Funding scheme Project funding
Research institution Département de Microbiologie Fondamentale Faculté de Biologie et de Médecine Université de Lausanne
Institution of higher education University of Lausanne - LA
Main discipline Experimental Microbiology
Start/End 01.04.2015 - 30.06.2018
Approved amount 429'000.00
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All Disciplines (6)

Discipline
Experimental Microbiology
Agricultural and Forestry Sciences
Molecular Biology
Genetics
Ecology
Immunology, Immunopathology

Keywords (11)

Insects; Microbes; Honey bee; Bee health; Symbiosis; Bacteria; Proteobacteria; Gut homeostasis; DNA damage; Pathogens; Gut microbiota

Lay Summary (German)

Lead
Honigbienen beherbergen eine einzigartige Bakteriengemeinschaft in ihrem Magendarmtrakt, welche sich im Laufe der Evolution spezifisch an diese Umgebung angepasst hat. Wie auch im Menschen können Magendarmbakterien der Honigbiene eine wichtige Rolle für die Gesundheit ihres Wirtes spielen. Die genauen Funktionen dieser Bakterien sind jedoch noch weitgehend unbekannt, trotz der zentralen Bedeutung von Bienen für natürliche Ökosysteme und die Landwirtschaft.
Lay summary

Das Kernziel dieses Forschungsprojektes wird es sein, die Interaktionen zwischen Bakterien und Honigbienen näher zu charakterisieren.  Hierzu werden keimfreie Bienen im Labor mit spezifischen Bakterienisolaten kolonisiert. Der Fokus wird auf Bakterien liegen, welche die Zellwände des Magendarmtraktes besiedeln und somit in enger Wechselwirkung mit dem Wirt stehen. Wir werden den Einfluss dieser Bakterien auf verschiedene Wirtsfaktoren, u.a. Immunsystem und Krankheitsresistenz, untersuchen. Des Weiteren werden wir genetische Faktoren dieser Bakterien bestimmen, welche für die Kolonisierung des Wirtes wichtig sind.

Als Bestäuber einer Vielzahl von Pflanzen ist die Honigbiene ein Insekt von zentraler Bedeutung für Umwelt und Landwirtschaft. Unsere Arbeit wird neue und wichtige Erkenntnisse über den Einfluss der Darmbakterien auf die Bienengesundheit aufdecken. Im Hinblick auf das weltweit vermehrte Auftreten von Bienensterben könnte dies zu neuen Strategien, zB. in der Bekämpfung und Prävention von Krankheiten, führen. Des Weiteren stellt die Honigbiene, auf Grund der einfachen Zusammensetzung ihrer Bakteriengemeinschaft im Magendarmtrakt, ein hervorragendes Model dar, um allgemeine Zusammenhänge zwischen Bakterien und Wirt zu untersuchen.  Unsere Forschung wird grundlegende Prinzipien dieser komplexen Wechselwirkungen aufzeigen.


Direct link to Lay Summary Last update: 25.03.2015

Responsible applicant and co-applicants

Employees

Publications

Publication
Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome
Hu Yi, Sanders Jon G., Łukasik Piotr, D’Amelio Catherine L., Millar John S., Vann David R., Lan Yemin, Newton Justin A., Schotanus Mark, Kronauer Daniel J. C., Pierce Naomi E., Moreau Corrie S., Wertz John T., Engel Philipp, Russell Jacob A. (2018), Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome, in Nature Communications, 9(1), 964-964.
Functional roles and metabolic niches in the honey bee gut microbiota
Bonilla-Rosso Germán, Engel Philipp (2018), Functional roles and metabolic niches in the honey bee gut microbiota, in Current Opinion in Microbiology, 43, 69-76.
Origin and Evolution of the Bartonella Gene Transfer Agent
Tamarit Daniel, Neuvonen Minna-Maria, Engel Philipp, Guy Lionel, Andersson Siv G E (2018), Origin and Evolution of the Bartonella Gene Transfer Agent, in Molecular Biology and Evolution, 35(2), 451-464.
Disentangling metabolic functions of bacteria in the honey bee gut
Kešnerová Lucie, Mars Ruben A. T., Ellegaard Kirsten M., Troilo Michaël, Sauer Uwe, Engel Philipp (2017), Disentangling metabolic functions of bacteria in the honey bee gut, in PLOS Biology, 15(12), e2003467-e2003467.
A bacterial toxin-antitoxin module is the origin of inter-bacterial and inter-kingdom effectors of Bartonella
Harms Alexander, Liesch Marius, Körner Jonas, Québatte Maxime, Engel Philipp, Dehio Christoph (2017), A bacterial toxin-antitoxin module is the origin of inter-bacterial and inter-kingdom effectors of Bartonella, in PLOS Genetics, 13(10), e1007077-e1007077.
Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen
Segers Francisca HID, Kešnerová Lucie, Kosoy Michael, Engel Philipp (2017), Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen, in The ISME Journal, 11(5), 1232-1244.
Immune system stimulation by the gut symbiont Frischella perrara in the honey bee ( Apis mellifera )
Emery Olivier, Schmidt Konstantin, Engel Philipp (2017), Immune system stimulation by the gut symbiont Frischella perrara in the honey bee ( Apis mellifera ), in Molecular Ecology, 26(9), 2576-2590.
Evolutionary Dynamics of Pathoadaptation Revealed by Three Independent Acquisitions of the VirB/D4 Type IV Secretion System in Bartonella
Harms Alexander, Segers Francisca H.I.D., Quebatte Maxime, Mistl Claudia, Manfredi Pablo, Körner Jonas, Chomel Bruno B., Kosoy Michael, Maruyama Soichi, Engel Philipp, Dehio Christoph (2017), Evolutionary Dynamics of Pathoadaptation Revealed by Three Independent Acquisitions of the VirB/D4 Type IV Secretion System in Bartonella, in Genome Biology and Evolution, 9(3), 761-776.
Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont
Powell J. Elijah, Leonard Sean P., Kwong Waldan K., Engel Philipp, Moran Nancy A. (2016), Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont, in Proceedings of the National Academy of Sciences, 113(48), 13887-13892.
Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota
Ellegaard Kirsten M., Engel Philipp (2016), Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota, in Frontiers in Microbiology, 7, 1475.

Collaboration

Group / person Country
Types of collaboration
Uwe Sauer Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Benjamin Dainat, Laurent Gauthier, Bee Research Centre, Liebefeld, CH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Ryo Miyazaki, National Institute of Advanced Industrial Science and Technology Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Prof. Jacob Russell, Drexel University United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Jan van der Meer (DMF) & Tadeusz Kawezki (DEE), University of Lausanne, CH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
Prof. Laurent Keller, DEE, University of Lausanne, CH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
4th Warwick Quantitative Biomedicine Symposium: Microbial communities: decoding interactions Individual talk Honey bee gut microbiota - versatile model for microbial symbiosis 04.06.2018 University of Warwick, UK, Great Britain and Northern Ireland Engel Philipp;
Seminar series Infection Biology Biozentrum Individual talk Honey bee Gut Microbiota - Versatile Model for Symbiosis 09.04.2018 Basel, Biozentrum, University of Basel, Switzerland Engel Philipp;
Seminar in course “Debating Science in Society” Individual talk Honey bee gut microbiota - Versatile model for microbial symbiosis 01.03.2018 ETHZ, Switzerland Engel Philipp;
Semester Opening Event (Science Slam) Mittelbauvereinigung Universität Bern Individual talk The honey bee gut microbiota: a tough place to live in 23.02.2018 Berne, Switzerland Schmidt Konstantin;
Survival Artist workshop Talk given at a conference Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen 09.10.2017 Marburg, Germany Engel Philipp;
Swiss Society for Microbiology meeting Poster Immune system stimulation by the gut symbiont Frischella perrara in the honey bee 01.09.2017 Basel, Switzerland Emery Olivier;
Joint EPFL/ETHZ PhD winter school Talk given at a conference Immune system stimulation by the gut symbiont Frischella 12.03.2017 Fiesch, Switzerland Emery Olivier;
ICE 2016 - Entomological Society of America Talk given at a conference The honey bee gut symbiont Frischella perrara: Friend or foe? 25.09.2016 Orlando, FL, United States of America Engel Philipp; Emery Olivier; Schmidt Konstantin;
8th Seeon conference on microbiota Talk given at a conference The honey bee gut microbiota - a versatile model for microbial symbiosis 25.06.2016 Seeon, Germany Engel Philipp;
Nature of Life Lecture Series Individual talk Honey bee gut microbiota - Versatile Model for Microbial Symbiosis 12.04.2016 Faculty of Earth and Life Sciences, Vrije Universiteit, Netherlands Engel Philipp;
Seminar Series in Evolutionary Biology Individual talk Honey bee Gut Microbiota - Diversity in Functions 26.10.2015 Department of Cell and Molecular Biology, University of Uppsala, Sweden Engel Philipp;
6th Swiss Microbial Ecology meeting Talk given at a conference Honey bee gut microbiota - Versatile model for microbial symbiosis 10.09.2015 Ascona, Switzerland Engel Philipp;
6th Swiss Microbial Ecology meeting Poster The gut symbiont Frischella perrara induces a specific immune response in its honey bee host 10.09.2015 Ascona, Switzerland Emery Olivier;
2nd Systems Biology of Infection Symposium Talk given at a conference Honey bee gut microbiota - Versatile model for microbial symbiosis 07.09.2015 Ascona, Switzerland Engel Philipp;
3rd Microbial Single Cell Genomics Workshop Talk given at a conference Comparative single cell genomics of honey bee gut symbionts 15.07.2015 Bigelow Laboratory, Maine, United States of America Engel Philipp;


Communication with the public

Communication Title Media Place Year
Media relations: radio, television Swiss French radio show “CQFD”, RSR radio station studio RSR Western Switzerland 2017

Associated projects

Number Title Start Funding scheme
189496 Evolutionary dynamics of the gut microbiome across honey bees 01.01.2021 SPIRIT
179487 Molecular crosstalk underlying symbiotic interactions in the honey bee gut microbiota 01.07.2018 Project funding
148264 Functional characterization of microbial symbioses in the honey bee gut microbiota 01.01.2014 Ambizione

Abstract

Gut microbial communities are important determinants of animal and human health. However, their complex composition displays a formidable challenge for studying symbiotic interactions in the gut. Simple model systems assist the discovery of fundamental principles of gut symbioses that are highly relevant to human health. The honey bee, Apis mellifera, represents such a model, because its gut microbiota consists of only eight bacterial species. These bacteria have long-standing evolutionary associations with their host suggesting important symbiotic roles that have largely remained elusive. Because honey bees are important pollinators suffering from severe population declines, a better understanding of factors influencing their health status is of broad interest, and the characteristic gut microbiota could be an important determinant.The main goals of this SNSF project are to study symbiotic roles of the gut microbiota affecting bee health (research objective 1) and to address general questions of gut microbiology (research objective 2). This research is based on my previous work in which I used genomic approaches to characterize the bee gut microbiota and established experimental tools for functional studies. We can culture now all bacterial members of the bee gut microbiota, generate microbiota-free bees, and re-colonize these bees with selected bacterial cultures. In the proposed research, this will allow us to study symbiotic interactions in a simple, but natural gut ecosystem of general relevance. Research objective 1 aims to elucidate the influence of the gut microbiota on pathogen susceptibility of honey bees. Together with a PhD student funded by this SNSF project, we will first establish colonization models in which we will transplant complete bacterial gut communities from conventional bees into microbiota-free bees (aim 1.1). We will then use these colonization models to test the influence of the gut microbiota on pathogen colonization and host resistance in controlled laboratory experiments (aim 1.2). Finally, we will identify bacterial community members contributing to identified symbiotic functions and study their underlying mechanisms of action (aim 1.3). Most studies focusing on honey bee health have not considered the influence of the gut microbiota and the proposed research will provide novel insights into the role of these bacteria. In the long run, our findings may contribute to the development of novel strategies to improve bee colony management. This makes our research not only relevant to basic science, but also to applied science supporting agricultural research and bee keeping industries.Research objective 2 will display a continuation of my Ambizione fellowship addressing more general aspects of gut microbiology. The focus of this research lies on Frischella perrara, a gammaproteobacterial gut symbiont, which colonizes a restricted niche in the bee gut and causes a remarkable host response, the deposition of melanin on the luminal surface of the gut. In addition, F. perrara encodes genes for the synthesis of a genotoxic small molecule that was shown for E. coli to cause DNA damage on eukaryotic cells and contribute to tumor formation in the human gut. Together with a second PhD student funded by this SNSF project, we will study the role of F. perrara for symbiosis in the bee gut, including its impact on gut homeostasis (aim 2.1) and host fitness (aim 2.2). We will analyze gene functions of F. perrara underlying symbiotic interactions in the bee gut (aim 2.3), and we will study the role of the genotoxic small molecule for symbiosis (aim 2.4). Taken together, the proposed work will address current questions of gut microbiology and honey bee health, combining two topics of biology and medical research which have recently received greatest attention. Due to its interdisciplinary nature, our research will interest a broad scientific community and is expected to receive international recognition. The main applicant and two PhD students funded by this grant will conduct the proposed research. We will collaborate with researchers at the University of Lausanne, the EPF Lausanne, the University of Berne, Agroscope Liebefeld, and Yale University. The SNSF project grant will replace my recently awarded SNSF Ambizione grant.
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