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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
Alumni
Publications
2019
FeaturedPrdx4 limits caspase-1 activation and restricts inflammasome-mediated signaling by extracellular vesicles
Lipinski S, Pfeuffer S, Arnold P, Treitz C, Aden K, Ebsen H, Falk-Paulsen M, Gisch N, Fazio A, Kuiper J, Luzius A, Billmann-Born S, Schreiber S, Nuñez G, Beer HD, Strowig T, Lamkanfi M, Tholey A, Rosenstiel P (2019) EMBO J. 38(20) doi: 10.15252/embj.2018101266.
FeaturedComparative analysis of amplicon and metagenomic sequencing methods reveals key features in the evolution of animal metaorganisms
Rausch P, Rühlemann M, Hermes BM, Doms S, Dagan T, Dierking K, Domin H, Fraune S, von Frieling J, Hentschel U, Heinsen F-A, Höppner M, Jahn MT, Jaspers C, Kissoyan KAB, Langfeldt D, Rehman A, Reusch TBH, Roeder T, Schmitz RA, Schulenburg H, Soluch R, Sommer F, Stukenbrock E, Weiland-Bräuer N, Rosenstiel P, Franke A, Bosch T, Baines JF (2019) Microbiome, doi: 10.1186/s40168-019-0743-1
FeaturedThe functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
Zimmermann J, Obeng N, Yang W, Pees B, Petersen C, Waschina S, Kissoyan KAB, Aidley J, Hoeppner MP, Bunk B, Spröer C, Leippe M, Dierking K, Kaleta C*, Schulenburg H* (2019) The ISME Journal. 1-13. * Shared senior authorship doi: 10.1038/s41396-019-0504-y
The inducible response of the nematode Caenorhabditis elegans to members of its natural microbiome across development and adult life
Yang W#, Petersen C#, Pees B#, Zimmermann J, Waschina S, Dirksen P, Rosenstiel P, Tholey A, Leippe M, Dierking K, Kaleta C*, Schulenburg H*. Front Microbiol. 10:1793. # Equal contribution as first authors, * Equal contribution as senior authors doi: 10.3389/fmicb.2019.01793.
aFold – using polynomial uncertainty modelling for differential gene expression estimation from RNA sequencing data
Yang W, Rosenstiel P, Schulenburg H (2019) BMC Genomics, 20:364, 1-17. doi: 10.1186/s12864-019-5686-1
A multi-parent recombinant inbred line population of C. elegans allows identification of novel QTLs for complex life-history traits
Snoek BL, Volkers RJM, Nijveen H, Petersen C, Dirksen P, Sterken MG, Nakad R, Riksen J, Rosenstiel P, Stastna JJ, Braeckman BP, Harvey SC, Schulenburg H*, Kammenga JE* (2019) BMC Biol. 17:24. * Shared senior authorship doi: 10.1186/s12915-019-0642-8
FeaturedNatural C. elegans microbiota protects against infection via production of a cyclic lipopeptide of the viscosin group
Kohar Kissoyan, Moritz Drechsler, Eva-Lena Stange, Johannes Zimmermann, Christoph Kaleta, Helge Bode und Katja Dierking (2019) Current Biology. DOI: 10.1016/j.cub.2019.01.050
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
The Caenorhabditis elegans proteome response to naturally associated microbiome members of the genus Ochrobactrum
Cassidy L, Petersen C, Treitz C, Dierking K, Schulenburg H, Leippe M, Tholey A (2018); Proteomics, doi: 10.1002/pmic.201700426
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
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