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Molecular basis and evolutionary dynamics of C. elegans-microbiota interactions

The model nematode Caenorhabditis elegans is associated with a distinct microbial community under natural conditions. Yet, to date, the role of the worm’s microbiota for life history functions and evolutionary fitness is largely unexplored. This collaborative project aims at providing a holistic understanding of C. elegans-microbiota interactions by
(i) dissecting the influence of the microbiota in mediating evolutionary adaptation to environmental stress using experimental evolution;
(ii) analysing the underlying genetics of C. elegans-microbiota interactions through QTL analysis, transcriptomics and functional genetic manipulation;
(iii) assessing the particular role of bioactive peptides and hydrolytic enzymes in shaping the nematode’s microbial associations using genetic and protein-level analyses; and
(iv) characterizing the proteomic basis of the interaction with the help of state-of-the-art proteome analysis techniques.

The proposed work is based on several advantages of the nematode as an experimental system, including the possibility of producing sterile nematodes through routine procedure combined with controlled re-infection experiments. The nematode also allows efficient performance of evolution experiments because of its short generation time and its amenability to cryopreservation for later analyses. Moreover, a versatile toolbox for genetic manipulation and comprehensive genome databases facilitate the cross-level “omics” analysis of C. elegans-microbiota interactions.

Overall, our project is unique in that it uses complementary study approaches and a highly efficient experimental model system to provide a holistic view on host-microbiota interactions that encompasses the involved evolutionary dynamics as well as the underlying processes at genomic, genetic, transcriptomic, proteomic and also biochemical levels. Based on such a cross-disciplinary analysis approach, our results are expected to yield novel insights into how the microbiota affects evolutionary change and how such dynamics are realized at the molecular level.

Researchers

Dr. Liam Cassidy

Postdoctoral Researcher, Alumni
Kiel University Institute for Experimental Medicine

Julia Johnke

Postdoctoral Researcher, Associated Junior Researcher
Kiel University Zoological Institute

Dr. Carola Petersen

Postdoctoral Researcher, Associated Junior Researcher
Kiel University Zoological Institute

Publications

2018

The Saposin-Like Protein AplD Displays Pore-Forming Activity and Participates in Defense Against Bacterial Infection During a Multicellular Stage of Dictyostelium discoideum.

Dhakshinamoorthy R, Bitzhenner M, Cosson P, Soldati T, Leippe M (2018); Front. Cell. Infect. Microbiol., 8:73. doi: 10.3389/fcimb.2018.00073

Miniaturized dispersive liquid-liquid microextraction and MALDI MS using ionic liquid matrices for the detection of bacterial communication molecules and virulence factors.

Leipert J, Bobis I, Schubert S, Fickenscher H, Leippe M, Tholey A (2018); Anal Bioanal Chem. , pp 1–12. doi: 10.1007/s00216-018-0937-6

Metaorganisms in extreme environments: do microbes play a role in organismal adaptation?

Bang C, Dagan T, Deines P, Dubilier N, Duschl W J, Fraune S, Hentschel U, Hirt H, Hülter N, Lachnit T, Picazo D, Galan P L, Pogoreutz C, Rädecker N, Saad M M, Schmitz R A, Schulenburg H, Voolstra C R, Weiland-Bräuer N, Ziegler M, Bosch T C G (2018); Zoology, doi: 10.1016/j.zool.2018.02.004

2017

We Are Not Alone: The iMOP Initiative and Its Roles in a Biology- and Disease-Driven Human Proteome Project.

Tholey A, Taylor N L, Heazlewood J L, Bendixen E (2017); J Proteome Res., 16(12):4273-4280. doi: 10.1021/acs.jproteome.7b00408

Insights into Microalga and Bacteria Interactions of Selected Phycosphere Biofilms Using Metagenomic, Transcriptomic, and Proteomic Approaches.

Krohn-Molt I, Alawi M, Förstner K U, Wiegandt A, Burkhardt L, Indenbirken D, Thieß M, Grundhoff A, Kehr J, Tholey A, Streit W R (2017); Front Microbiol., doi: 10.3389/fmicb.2017.01941

Identification and Quantification of N-Acyl Homoserine Lactones Involved in Bacterial Communication by Small-Scale Synthesis of Internal Standards and Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry.

Leipert J, Treitz C, Leippe M, Tholey A (2017); J Am Soc Mass Spectrom., 28(12):2538-2547. doi: 10.1007/s13361-017-1777-x

The Natural Biotic Environment of Caenorhabditis elegans.

Schulenburg H, Félix M A (2017); Genetics., 206(1):55-86. doi: 10.1534/genetics.116.195511

The Natural Biotic Environment of Caenorhabditis elegans.

Schulenburg H, Félix M A (2017); Genetics., 206(1):55-86. doi: 10.1534/genetics.116.195511

Caenorhabditis elegans as a model for microbiome research.

Zhang F, Berg M, Dierking K, Félix M A, Shapira M, Samuel B, Schulenburg H (2017); Front. Microbiol., 8:485. doi: 10.3389/fmicb.2017.00485

FeaturedEfficacy of Sterile Fecal Filtrate Transfer for Treating Patients With Clostridium difficile Infection. Gastroenterology.

Ott S J, Waetzig G H, Rehman A, Moltzau-Anderson J, Bharti R, Grasis J A, Cassidy L, Tholey A, Fickenscher H, Seegert D, Rosenstiel P, Schreiber S (2017); Gastroenterology, 152(4):799-811.e7. doi: 10.1053/j.gastro.2016.11.010

2016

Differential quantitative proteome analysis of Escherichia coli grown on acetate versus glucose.

Treitz C, Enjalbert B, Portais J C, Letisse F, Tholey A (2016); Proteomics., 16(21):2742-2746. doi: 10.1002/pmic.201600303

Combination of Bottom-up 2D-LC-MS and Semi-top-down GelFree-LC-MS Enhances Coverage of Proteome and Low Molecular Weight Short Open Reading Frame Encoded Peptides of the Archaeon Methanosarcina mazei.

Cassidy L, Prasse D, Linke D, Schmitz R A, Tholey A (2016)
J Proteome Res., 15(10):3773-3783. doi: 10.1021/acs.jproteome.6b00569

Antimicrobial effectors in the nematode C. elegans – an outgroup to the Arthropoda.

Dierking K, Yang W, Schulenburg H (2016); Phil Trans R Soc Lond B., 371. doi:

The native microbiome of the nematode Caenorhabditis elegans: Gateway to a new host-microbiome model.

Dirksen P, Marsh SA, Braker I, Heitland N, Wagner S, Nakad R, Mader S, Petersen C, Kowallik V, Rosenstiel P C, Felix M A, Schulenburg H (2016); BMC Biology, 14:38. doi:10.1186/s12915-016-0258-1