A1
Evolution and Ecology

Evolutionary dynamics and molecular basis of C. elegans-microbiome interactions

Microorganisms play a central role in the biology of multicellular organisms and have shaped their evolution from the very beginning. However, we still lack precise information on how the microbiome mediates evolutionary adaptation and how exactly it affects key biological functions such as host metabolism and defense against pathogens. The A1 project uses the nematode Caenorhabditis elegans as a versatile experimental model system to address current knowledge gaps in these areas.

In the second funding period of the CRC, we established that both host and microbes contribute to evolutionary fitness of the metaorganism in a novel environment. Moreover, we identified sphinganine as a microbiome-derived, protective metabolite, and found that modification of host sphingolipid metabolism affects C. elegans resistance to pathogens. We further implemented an integrated metabolic network model of C. elegans and selected bacterial species to pinpoint specific metabolic pathways involved in host-microbe interactions and developed a proof-of-principle approach for a targeted modulation of microbial community composition.

Based on these insights, the overarching objectives of the A1 project in the third funding phase are to enhance our understanding of microbiome-mediated adaptation and the molecular and metabolic processes involved in metaorganism evolution and protection against pathogen infection.

We will (i) perform a quantitative genetic analysis of microbiome-mediated host adaptation (A1.1, PI Schulenburg),

(ii) study how microbiome-derived sphinganine affects host sphingolipid metabolism and pathogen defense (A1.2, PI Dierking), and

(iii) use metabolic modeling to identify conserved metabolic microbiome-host-interactions and explore them in the C. elegans system (A1.5, PI Kaleta).

The objectives are achieved through collaborative interactions within the A1 project, as established during the previous funding phases, combining and integrating expertise in evolutionary genetics (PI Schulenburg), genetics and immunology (PI Dierking), and systems biology (PI Kaleta).

The proposed project is one of the first to quantify the relative contributions of host genetics and microbiome to adaptation, using a refined quantitative genetics framework. It provides novel insights into the precise function of microbiome- as well as host-derived sphingolipids in protection against pathogens. It is also unique in yielding an integrated host-microbiome metabolic network model that provides a predictive framework for manipulating community composition and resulting microbiome functions.

A1
Researchers

Researchers

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A1.1: Evolution of microbiome-mediated effects on host fitness

A1.2: Molecular basis of microbiome-mediated protection against pathogen infection

A1.5: Metabolic modeling of host-microbiome-interactions

A1
Related Publications

Related Publications

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2024
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A4

Gut-associated functions are favored during microbiome assembly across a major part of C. elegans life

Johannes Zimmermann, Agnes Piecyk, Michael Sieber, Carola Petersen, Julia Johnke, Lucas Moitinho-Silva, Sven Künzel, Lena Bluhm, Arne Traulsen, Christoph Kaleta, Hinrich Schulenburg (2024): Gut-associated functions are favored during microbiome assembly across a major part of C. elegans life. MBio First published: 18. April 2024
DOI: 10.1128/mbio.00012-24

2023
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C2

Recurrent phases of strict protein limitation inhibit tumor growth and restore lifespan in a Drosophila intestinal cancer model.

Pfefferkorn RM, Mortzfeld BM, Fink C, von Frieling JBossen J, Esser D, Kaleta CRosenstiel P, Heine H, Roeder T (2023) Recurrent phases of strict protein limitation inhibit tumor growth and restore lifespan in a Drosophila intestinal cancer model. Aging&Disease in press.

2023
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The nematode Caenorhabditis elegans and diverse potential invertebrate vectors predominantly interact opportunistically

The nematode Caenorhabditis elegans and diverse potential invertebrate vectors predominantly interact opportunistically.
Petersen C, Krahn A, Leippe M. (2023) Front. Ecol. Evol.
doi: 10.3389/fevo.2023.1069056
2023
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INF

Gut-associated functions are favored during microbiome assembly across C. elegans life

Zimmermann J*, Piecyk A*, Sieber M, Petersen C, Johnke J, Moitinho-Silva L, Künzel S, Bluhm L, Traulsen A, Kaleta C, Schulenburg H (2023) Gut-associated functions are favored during microbiome assembly across C. elegans life. bioRxiv doi:10.1101/2023.03.25.534195. *Shared first authorship.

2023
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INF
Z3

Host and microbiome jointly contribute to environmental adaptation

Petersen C*, Hamerich IK*, Adair KL*, Griem-Krey H, Torres Oliva M, Hoeppner MP, Bohannan BJM*, Schulenburg H* (2023) Host and microbiome jointly contribute to environmental adaptation. ISME Journal doi.org/10.1038/s41396-023-01507-9. *Shared first or senior authorship.

2023
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The intricate triangular interaction between protective microbe, pathogen, and host genetics determines fitness of the metaorganism

Griem-Krey H*, Petersen C*, Hamerich IK, Schulenburg H (2023) The intricate triangular interaction between protective microbe, pathogen, and host genetics determines fitness of the metaorganism. bioRxiv *shared first authors doi:10.1101/2023.03.22.533850.

2023
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The C. elegans proteome response to two protective Pseudomonas symbionts

Barbara Pees*, Lena Peters, Christian Treitz, Inga K. Hamerich, Kohar A. B. Kissoyan, Andreas Tholey, Katja Dierking* (2023) The C. elegans proteome response to two protective Pseudomonas symbionts. bioRxiv doi:10.1101/2023.03.22.533766. *Shared corresponding authors.

2023
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Closely related Bacteroides of the murine intestinal microbiota affect each other’s growth positively or negatively

Hanna Fokt, Gabija Sakalyte, Rahul Unni, Mohammad Abukhalaf, Liam Cassidy, Georgios Marinos, Maxime Godfroid, Birhanu M Kinfu, Ruth A Schmitz, Christoph Kaleta, Andreas Tholey, John F Baines, Tal Dagan, Daniel Unterweger (2023) BioRxiv
2023
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Metabolic model predictions enable targeted microbiome manipulation through precision prebiotics

Marinos G, Hamerich I K, Debray R, Obeng N, Petersen C, Taubenheim J, Zimmermann J, Blackburn D, Samuel B S, Dierking K, Franke A, Laudes M, Waschina S, Schulenburg H, Kaleta D. (2023) bioRxiv, 

2023
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INF
Z2

Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis

Domin H, Zimmermann J, Taubenheim J, Fuentes Reyes G, Saueressig L, Prasse D, Höppner M, Schmitz RA, Hentschel U, Kaleta C, Fraune S (2023) Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis. Microbiome doi:10.1186/s40168-023-01701-z

 

 

 

 

2022
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Isolation and Characterization of the Natural Microbiota of the Model Nematode Caenorhabditis elegans

Petersen, C., Dierking, K., Johnke, J., Schulenburg, H. Isolation and Characterization of the Natural Microbiota of the Model Nematode Caenorhabditis elegans. J. Vis. Exp. (186), e64249, doi:10.3791/64249 (2022).

2022
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Exploring Effects of C. elegans Protective Natural Microbiota on Host Physiology.

Kissoyan KAB, Peters L, Giez C, Michels J, Pees B, Hamerich IK, Schulenburg H, Dierking K. (2022) Front Cell Infect Microbiol. 12:775728. doi: 10.3389/fcimb.2022.775728
2021
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Preconditioning with natural microbiota strain Ochrobactrum vermis MYb71 influences Caenorhabditis elegans behavior

Petersen C, Pees B, Martínez Christophersen C, Leippe M (2021) Front Cell Infect Microbiol. 11:775634. doi: 10.3389/fcimb.2021.775634
2021
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In vitro interaction network of a synthetic gut bacterial community.

Weiss AS, Burrichter AG, Durai Raj AC, von Strempel A, Meng C, Kleigrewe K, Münch PC, Rössler L, Huber C, Eisenreich W, Jochum LM, Göing S, Jung K, Lincetto C, Hübner J, Marinos G, Zimmermann J, Kaleta C, Sanchez A, Stecher B (2021)  ISME J. doi: 1038/s41396-021-01153-z

2021
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Microbial regulation of hexokinase 2 links mitochondrial metabolism and cell death in colitis.

Hinrichsen F, Hamm J, Westermann M, Schröder L, Shima K, Mishra N, Walker A, Sommer N, Klischies K, Prasse D, Zimmermann J, Kaiser S, Bordoni D, Fazio A, Marinos G, Laue G, Imm S, Tremaroli V, Basic M, Häsler R, Schmitz RA, Krautwald S, Wolf A, Stecher B, Schmitt-Kopplin P, Kaleta C, Rupp J, Bäckhed F, Rosenstiel P, Sommer F (2021) Cell Metab 33(12):2355-2366.e8. doi: 1016/j.cmet.2021.11.004

2021
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Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria

Giri S, Oña L, Waschina S, Shitut S, Yousif G, Kaleta C, Kost C (2021) Curr Biol. S0960-9822(21)01408-1. doi: 1016/j.cub.2021.10.019.

2021
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Microbes to-go: slugs as source for Caenorhabditis elegans microbiota acquisition.

Pees B, Johnke J, Möhl M, Hamerich IK, Leippe M, Petersen C (2021) Environ. Microbiol. doi:10.1111/1462-2920.15730.

2021
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INF

The genetics of gene expression in a Caenorhabditis elegans multiparental recombinant inbred line population.

Snoek BL, Sterken MG, Nijveen H, Volkers RJM, Riksen J, Rosenstiel PC, Schulenburg H, Kammenga JE. (2021) G3 (Bethesda). 11(10):jkab258. doi: 10.1093/g3journal/jkab258.

2021
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The effects of nested miRNAs and their host genes on immune defense against Bacillus thuringiensis infection in Caenorhabditis elegans.

Zárate-Potes A, Yang W, Andresen B, Nakad B, Haase D, Rosenstiel P, Dierking K*, Schulenburg H* (2021) Dev Comp Immunol. 123:104144 doi: 10.1016/j.dci.2021.104144  *Shared senior authorship.

2021
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Effector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins.

Pees B, Yang W, Kloock A, Petersen C, Peters L, Fan L, Friedrichsen M, Butze S, Zárate-Potes A, Schulenburg H, Dierking K (2021)  PLoS Pathogens. 17(4):e1009454. doi: 10.1371/journal.ppat.1009454

2021
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gapseq: informed prediction of bacterial metabolic pathways and reconstruction of accurate metabolic models

Zimmermann J, Kaleta C, Waschina S (2021) Genome Biol. 22(81):1-35. doi: 10.1186/s13059-021-02295-1

2020
A1

Defining the nutritional input for genome-scale metabolic models: a roadmap

Marinos G, Kaleta C, Waschina S (2020) PLOS ONE 15(8): e0236890. doi: 10.1371/journal.pone.0236890

2020
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Microbiome-mediated plasticity directs host evolution along several distinct time scale

Kolodny O, Schulenburg H (2020) Phil. Trans. R. Soc. B. 375: 20190589. doi: 10.1098/rstb.2019.0589

2020
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PR

Metaorganismusforschung trifft Schule: Wissenschaftskommunikation an der Universität zu Kiel.

Claussen C, Kapitza M, Knapp JM, Bernholt A, Schulenburg H, Kremer KH (2020). Biologie in unserer Zeit (BiuZ), 50(4), 270-277. doi: 10.1002/biuz.202010713

2020
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CeMbio – The Caenorhabditis elegans microbiome resource

Dirksen P, Assié A, Zimmermann J, Zhang F, Tietje A-M, Arnaud Marsh S, Félix M-A, Shapira M, Kaleta C, Schulenburg H, Samuel B (2020)
2020
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B1

Receptors mediating host-microbiota communication in the metaorganism: the invertebrate perspective.

Dierking K, Pita L (2020) Front. Immunol. 11:1251. doi: 10.3389/fimmu.2020.01251

2020
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The 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) ISME J. 14: 26–38. * Shared first or senior authorship  doi: 10.1038/s41396-019-0504-y

2019
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C2

Prdx4 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.

2019
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Comparative 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

2019
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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.

2019
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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

2019
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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

2019
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Natural 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
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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

2018
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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

2018
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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

2018
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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
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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

2017
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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

2017
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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

2017
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The Natural Biotic Environment of Caenorhabditis elegans.

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

2017
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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

2017
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Efficacy 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
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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

2016
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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

2016
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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

2016
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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:

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