A1
Evolution and Ecology

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

The association between a host and its microbiome is of central importance for life-history and evolutionary potential of the interacting organisms. Yet, we still have comparatively little understanding of the exact selective processes and resulting evolutionary consequences of these interactions. Adaptation to environmental stress may be facilitated through the interaction, for example if microbes enable the host to survive a harmful environmental condition and thereby the entire association of interacting organisms, the metaorganism, is able to persist. This beneficial interaction is likely to rely on the metabolic competences of the involved organisms and the exchange of nutrients and other substances. A better understanding of both the evolutionary processes and the underlying molecular and metabolic basis may be obtained with the help of an experimentally accessible host system. The model nematode Caenorhabditis elegans provides such a system. This nematode is associated with a speciesrich community of bacteria, most of which can also be easily maintained in culture.

In the first funding period, we established that an important function of the C. elegans microbiota is protection against pathogens. Based on omics approaches and metabolic network models, we further found that the individual members of the microbial community vary in their metabolic activities, thereby influencing key aspects of the host-microbiome interaction, for example colonization ability of the bacteria and C. elegans population growth.

Based on these insights, the overarching objectives of the A1 project in the second funding period will be to enhance our understanding of the evolution of microbiota-mediated protection against pathogen stress and the molecular and metabolic processes involved.

We will (1) experimentally test the influence of the microbiome on evolutionary adaptation of the C. elegans metaorganism to pathogens (A1.1, PI Schulenburg),

(2) study the molecular basis of microbiota-mediated protection against pathogens using functional genetics (A1.2, PI Dierking), and

(3) assess which metabolic pathways mediate the interaction between C. elegans and its microbiome during evolutionary adaptation and immune protection (A1.5, PI Kaleta).

The A1 PIs have complementary research competences (HS: evolution and ecology of C. elegans; KD: C. elegans immunity and signalling; CK: modelling of C. elegans and microbial metabolism), which will be combined across the subprojects. The proposed project is thus one of the first to experimentally test the role of the microbiome on evolutionary adaptation, using evolution experiments combined with omics, functional genetics, and metabolic modelling approaches. It is one of the very few to provide in-depth information on the genetic and molecular basis of distinct types of microbiota-mediated immune protection. It is also one of the first to explore and experimentally validate the interconnectivity of host and microbiome metabolic networks and its consequences for the resulting phenotypes.

This project exploits the advantages of the C. elegans model for a controlled interdisciplinary research agenda, in order to disentangle cause-effect relationships that define the evolution and function of a metaorganism.

A1
Researchers

Researchers

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

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

A1.5: Metabolic modelling of hostmicrobiota-interactions

A1: Alumni

A1
Related Publications

Related Publications

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Year All
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
A1
A4

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

2020
A1

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
A1
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

2019
A1
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
A1
A2
A3
B1
B2
C1
C2
INF
Z3

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
A1
A4
INF

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) The ISME Journal. 1-13. * Shared first or senior authorship  doi: 10.1038/s41396-019-0504-y

2019
A1
A4
INF
Z3

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
A1

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
A1

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
A1

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
A1

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
A1

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
A1

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
A1
A2
A3
A4
B1
B2
C1
Z1
Z2

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
A1

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
A1

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
A1

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
A1
A4

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
A1
A4

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
A1
C2
Z3

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
A1

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
A1
B2
Z2

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
A1
A4
C2
Z3

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
A1
A4

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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