A2
Evolution and Ecology

Host-microbiota coevolution in the mammalian intestine

This project aims to determine the genetic basis of evolutionary change among mammalian metaorganisms. Through the use of highly sophisticated and unique genetic resources in both the house mouse subspecies complex and humans, we identified highly interesting candidate host loci and microbial taxa that may be involved in adaptation by one or both partners. Common aspects that emerged from both model systems are host genes involved in circadian rhythms and bacterial taxa belonging to Bacteroides.

In the second funding period we will conduct a thorough functional characterization of the most influential candidate host genes and bacterial taxa. This includes the pinpointing of causative mutations, the use of knockout mouse models and the characterization of bacterial strain-level variation. Further, we will improve upon 16S rRNA gene-based mapping by extending mapping efforts to the level of functional elements of the gut microbiome, using shotgun metagenomic sequencing. Importantly, the shotgun metagenomic data will also enable us to extend mapping to non-bacterial elements of the gut microbiome, including novel archaeal taxa in mice.

The A2 project is comprised of a unique combination of evolutionary microbiome research, microbiology and state of the art genetic mapping analysis. The latter is made possible by one-of-a-kind mouse genetic resources and being lead participants in international consortia. Accordingly, our project is the first to clearly identify genetic variation in circadian processes as an aspect of ongoing evolutionary dynamics in mammalian metaorganisms, which will be explored in detail in this funding period.

The overall goal of our project is to identify and characterize the genetic basis of evolutionary change between mammalian metaorganisms. Using the house mouse species complex (A2.1, PI Baines) and Hominidae systems (A2.2, PI Franke), we hypothesize that mammals share themes and mechanisms of host-microbe interaction.

Accordingly, the main joint aims of the first funding period were to (i) identify host genomic regions influencing microbial traits by employing genetic mapping approaches, (ii) perform a fine-scale characterization of candidate bacterial taxa at the genomic level, (iii) identify signatures of coadaptation via population genetic and comparative genomic analyses. This work yielded many interesting results, which importantly include overlap in host genes and bacterial taxa between the two model systems.

A2
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A2
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2023
A2
C2
Z3

A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression

Knop M, Treitz C, Bettendorf S, Bossen J, von Frieling J, Doms S, Bruchhaus I, Kuehnlein RP, Baines JF, Tholey A, Roeder T (2023) A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression. bioRxiv, doi: https://doi.org/10.1101/2023.06.02.543385

2023
A2
B2
B4

Comparative genomics of novel Bacteroides acidifaciens isolates reveals candidates for adaptation to host subspecies in house mice

Hanna Fokt, Shauni Doms, Malte C. Rühlemann, Maxime Godfroid, Ruth A. Schmitz, Britt M. Hermes, John F. Baines (2023) Comparative genomics of novel Bacteroides acidifaciens isolates reveals candidates for adaptation to host subspecies in house mice BioRxiv

 

2023
A2
A4
C1
C2

The microbiome of the marine flatworm Macrostomum lignano provides fitness advantages and exhibits circadian rhythmicity

Ma YHe JSieber Mvon Frieling J, Bruchhaus I, Baines JF, Bickmeyer U, Roeder T (2023) The microbiome of the marine flatworm Macrostomum lignano provides fitness advantages and exhibits circadian rhythmicity. Communications Biology 6: 289. https://doi.org/10.1038/s42003-023-04671-y.

2023
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B2
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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
A2
C2
Z3

A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression

Knop M, Treitz C, Bettendorf S, Bossen J, von Frieling J, Doms S, Bruchhaus I, Kuehnlein RP, Baines JF, Tholey ARoeder T (2023) A mitochondrial sirtuin shapes the intestinal microbiota by controlling lysozyme expression. bioRxiv, doi: https://doi.org/10.1101/2023.06.02.543385

2023
A1
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A4

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
A2
Z3

Pathometagenomics reveals susceptibility to intestinal infection by Morganella to be mediated by the blood group-related B4galnt2 gene in wild mice

Marie Vallier, Abdulhadi Suwandi, Katrin Ehrhardt, Meriem Belheouane, David Berry, Aleksa Čepić, Alibek Galeev, Jill M. Johnsen, Guntram A. Grassl, and John F. Baines (2023): GUT MICROBES , VOL. 15, NO. 1, 2164448
https://doi.org/10.1080/19490976.2022.2164448

 

2022
A2
B4
Z2

Bacteroides muris sp. nov. isolated from the cecum of wild-derived house mice.

Hanna Fokt, Rahul Unni, Urska Repnik, Ruth A. Schmitz, Marc Bramkamp, John F. Baines, Daniel Unterweger. Archives of Microbiology 204:546.
doi: 10.1007/s00203-022-03148-6

2022
A2
Z3

Key features of the genetic architecture and evolution of host-microbe interactions revealed by high-resolution genetic mapping of the mucosa-associated gut microbiome in hybrid mice

Doms S, Fokt H, Ruehlemann MC, Chung CJ, Kuenstner A, Ibrahim S, Franke A, Turner LM, Baines JF (2022):  eLife; 11:e75419. doi: 10.7554/eLife.75419

2022
A2
C2

DNA methyltransferase 3A controls intestinal epithelial barrier function and regeneration in the colon

Fazio A, Bordoni D, Kuiper JWP, Franke A, Rosenstiel P. et al. DNA methyltransferase 3A controls intestinal epithelial barrier function and regeneration in the colon. Nat Commun 13, 6266 (2022). https://doi.org/10.1038/s41467-022-33844-2

 

2021
A2

Ecology impacts the decrease of Spirochaetes and Prevotella in the fecal gut microbiota of urban humans

Thingholm LB, Bang C, Rühlemann MC, Starke A, Sicks F, Kaspari V, Jandowsky A, Frölich K, Ismer G, Bernhard A, Bombis C, Struve B, Rausch P, Franke A (2021) BMC Microbiol. 21:276. doi: 10.1186/s12866-021-02337-5

2021
A2

Primate phageomes are structured by superhost phylogeny and environment.

Gogarten, JF, Rühlemann M, Archie E, Tung J, Akoua-Koffi C, Bang C, Deschner T, Muyembe-Tamfun J-J, Robbins MM, Schubert G, Surbeck M, Wittig RM, Zuberbühler K, Baines JF, Franke A, Leendertz FH, Calvignac-Spencer S, 

2021
A2

Large-scale association analyses identify host factors influencing human gut microbiome composition.

Kurilshikov A, Medina-Gomez C, Bacigalupe R,…Rühlemann MC,Bang C,…Franke A,… et al. (2021) Nat Genet 53:156–165. doi: 10.1038/s41588-020-00763-1

2021
A2
INF

Genome-wide association study in 8,956 German individuals identifies influence of ABO histo-blood groups on gut microbiome.

Rühlemann MC, Hermes BM, Bang C, Doms S, Moitinho-Silva L, Thingholm LB, Frost F, Degenhardt F, Wittig M, Kässens J, Weiss FU, Peters A, Neuhaus K, Völker U, Völzke H, Homuth G, Weiss S, Laudes M, Lieb W, Haller D, Lerch MM, Baines JF, Franke A (2021) Nat Genet. 53, 147–155. doi: 10.1038/s41588-020-00747-1

2020
A2

S100A8 and S100A9 Are Important for Postnatal Development of Gut Microbiota and Immune System in Mice and Infants.

Willers M, Ulas T, Völlger L, Vogl T, Heinemann AS, Pirr S, Pagel J, Fehlhaber B, Halle O, Schöning J, Schreek S, Löber U, Essex M, Hombach P, Graspeuntner S, Basic M, Bleich A, Cloppenborg-Schmidt K, Künzel S, Jonigk D, Rupp J, Hansen G, Förster R, Baines JF, Härtel C, Schultze JL, Forslund SK, Roth J, Viemann D (2020)  Gastroenterology. 159(6):2130-2145.e5. doi: 1053/j.gastro.2020.08.019.

2020
A2

Genome-wide associations of human gut microbiome variation and implications for causal inference analyses

Hughes DA, Bacigalupe R, Wang J, Rühlemann MC, Tito RY, Falony G, Rymenans L, Verspecht C, Ring S, Franke A, Wade KH, Timpson NJ, Raes J (2020) Nat Microbiol 5, 1079–1087. doi: 10.1038/s41564-020-0743-8
2020
A2

Assessing similarities and disparities in the skin microbiota between wild and laboratory populations of house mice

Belheouane M, Vallier M, Čepić A, Chung CJ, Ibrahim S, Baines FJ (2020) ISME J. 14, 2367–2380 doi: 10.1038/s41396-020-0690-7

2020
A2
B2

Differences in the microbiota of native and non-indigenous gelatinous zooplankton organisms in a low saline environment

Jaspers C, Weiland-Bräuer N, Rühlemann MC, Baines JF, Schmitz RA, Reusch TBH (2020) Sci Total Environ. 734:139471. doi: 10.1016/j.scitotenv.2020.139471

2020
A2

A disease‐specific decline of the relative abundance of Bifidobacterium in patients with autoimmune hepatitis

Liwinski T, Casar C, Ruehlemann MC, Bang C, Sebode M, Hohenester S, Denk G, Lieb W, Lohse AW, Franke A, Schramm C (2020) Aliment Pharmacol Ther. 51(12):1417-1428. doi: 10.1111/apt.15754
2020
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A3

A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition

Seybold H, Demetrowitsch TJ, Hassani M A, Szymczak S, Reim E, Haueisen J, Lübbers L, Rühlemann M, Franke A, Schwarz k, H. Stukenbrock E (2020) Nature Communications. 11(1):1910. doi: 10.1038/s41467-020-15633-x

2020
A2
C2
Z3

NOD2 influences trajectories of intestinal microbiota recovery after antibiotic perturbation

Moltzau Anderson J, Lipinski S, Sommer F, Pan W-H, Boulard O, Rehman A, Falk-Paulsen M, Stengel ST, Aden K, Häsler R, Bharti R, Künzel S, Baines JF, Chamaillard M, Rosenstiel P (2020) Cell Mol Gastroenterol Hepatol. 10(2): 365-389. doi: 10.1016/j.jcmgh.2020.03.008

2020
A2

Alterations of the bile microbiome in primary sclerosing cholangitis

Liwinski T, Zenouzi R, John C, Ehlken H, Rühlemann MC, Bang C,  Groth S, Lieb W, Kantowski M, Andersen N, Schachschal G, Karlsen TH, Hov JH, Rösch T, Lohse AW, Heeren J, Franke A, Schramm C (2020) Gut 69 (4), 665-672 doi: 10.1136/gutjnl-2019-318416
2020
A2

An integrated metagenome catalog reveals new insights into the murine gut microbiome

Lesker TR, Durairaj AC, Gálvez EJC, Lagkouvardos I, Baines JF, Clavel T, Sczyrba A, McHardy AC, Strowig T (2020) Cell Rep. 30(9): 2909–2922.e6. doi: 10.1016/j.celrep.2020.02.036

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
A2

Consistent alterations in faecal microbiomes of patients with primary sclerosing cholangitis independent of associated colitis

Rühlemann M, Liwinski T, Heinsen F-A, Bang C, Zenouzi R, Kummen M, Thingholm L, Tempel M, Lieb W, Karlsen T, Lohse A, Hov J, Denk G, Lammert F, Krawczyk M, Schramm C, Franke A (2019) Aliment Pharmacol Ther. 1-10. doi: 10.1111/apt.15375

2019
A2

Alterations of the bile microbiome in primary sclerosing cholangitis

Liwinski T, Zenouzi R, John C, Ehlken H, Rühlemann MC, Bang C, Groth S, Lieb W, Kantowski M, Andersen N, Schachschal G, Karlsen TH, Hov JR, Rösch T, Lohse AW, Heeren J, Franke A, Schramm C (2019) Gut 0:1–8. doi:10.1136/gutjnl-2019-318416

2019
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A4
B1
B2

Neutrality in the metaorganism

Sieber M, Pita L, Weiland-Bräuer N, Dirksen P, Wang J, Mortzfeld B, Franzenburg S, Schmitz RA, Baines JF, Fraune S, Hentschel U, Schulenburg H, Bosch TCG, Traulsen A (2019) PLoS Biol., DOI: 10.1371/journal.pbio.3000298

2019
A2

Sequence and cultivation study of Muribaculaceae reveals novel species, host preference, and functional potential of this yet undescribed family

Lagkouvardos I, Lesker TR, Hitch TCA, Gálvez EJC, Smit N, Neuhaus K, Wang J, Baines JF, Abt B, Stecher B, Overmann J, Strowig T, Clavel T. (2019) Microbiome 7(1):28. doi: 10.1186/s40168-019-0637-2

2018
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B2
C1
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INF
Z2

Functions of the Microbiota for the Physiology of Animal Metaorganisms

Esser D, · Lange J, · Marinos G, · Sieber M, Best L, Prasse D, Bathia J, Rühlemann MC, Boersch K, Jaspers C, Sommer F (2018) J Innate Immun DOI: 10.1159/000495115

2018
A2
C2

Exposure to the gut microbiota drives distinct methylome and transcriptome changes in intestinal epithelial cells during postnatal development

Franke A, Schultze JL, Bäckhed F, Rosenstiel P (2018) Genome Med. 10(1):27. doi: 10.1186/s13073-018-0534-5.
2018
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Z3

Low-level mitochondrial heteroplasmy modulates DNA replication, glucose metabolism and lifespan in mice.

Hirose M, Schilf P, Gupta Y, Zarse K, Künstner A, Fähnrich A, Busch H, Yin J, Wright MN, Ziegler A, Vallier M, Belheouane M, Baines JF, Tautz D, Johann K, Oelkrug R, Mittag J, Lehnert H, Othman A, Jöhren O, Schwaninger M, Prehn C, Adamski J, Shima K, Rupp J, Häsler R, Fuellen G, Köhling R, Ristow M, Ibrahim SM (2018); Sci Rep. 8(1):5872. doi: 10.1038/s41598-018-24290-6

2018
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C2
INF
Z3

Exposure to the gut microbiota drives distinct methylome and transcriptome changes in intestinal epithelial cells during postnatal development.

Pan WH, Sommer F, Falk-Paulsen M, Ulas T, Best P, Fazio A, Kachroo P, Luzius A, Jentzsch M, Rehman A, Müller F, Lengauer T, Walter J, Künzel S, Baines JF, Schreiber S, Franke A, Schultze JL, Bäckhed F, Rosenstiel P (2018); Genome Med. 10(1):27. doi: 10.1186/s13073-018-0534-5

2018
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Z3

The evolution of ecological facilitation within mixed-species biofilms in the mouse gastrointestinal tract.

Lin XB, Wang T, Stothard P, Corander J, Wang J, Baines JF, Knowles SCL, Baltrūnaitė L, Tasseva G, Schmaltz R, Tollenaar S, Cody LA, Grenier T, Wu W, Ramer-Tait AE, Walter J (2018); ISME J. doi: 10.1038/s41396-018-0211-0

2018
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B1
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Z2

The sponge holobiont in a changing ocean: from microbes to ecosystems.

Pita L, Rix L, Slaby B M, Franke A, Hentschel U (2018); Microbiome, 6(46). doi: 10.1186/s40168-018-0428-1

2018
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Epidermal lipid composition, barrier integrity, and eczematous inflammation are associated with skin microbiome configuration

Baurecht H, Rühlemann M, Rodríguez E, Thielking F, Harder I, Erkens AS, Stölzl D, Ellinghaus E, Hotze M, Lieb W, Wang S, Heinsen FA, Franke A, Weidinger S (2018) J ALLERGY CLIN IMMUN . doi: 10.1016/j.jaci.2018.01.019

2018
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C2
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Z3

The antibiotic resistome and microbiota landscape of refugees from Syria, Iraq and Afghanistan in Germany.

Häsler R, Kautz C, Rehman A, Podschun R, Gassling V, Brzoska P, Sherlock J, Gräsner J T, Hoppenstedt G, Schubert S, Ferlinz A, Lieb W, Laudes M, Heinsen F A, Scholz J, Harmsen D, Franke A, Eisend S, Kunze T, Fickenscher H, Ott S, Rosenstiel P, Schreiber S (2018); Microbiome., 6(1):37. doi: 10.1186/s40168-018-0414-7

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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Application of the distance-based F test in an mGWAS investigating β diversity of intestinal microbiota identifies variants in SLC9A8 (NHE8) and 3 other loci.

Rühlemann M C, Degenhardt F, Thingholm L B, Wang J, Skiecevičienė J, Rausch P, Hov J R, Lieb W, Karlsen T H, Laudes M, Baines J F, Heinsen F A, Franke A (2017); Gut Microbes., 8:55. doi: 10.1080/19490976.2017.1356979

2016
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C2
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Z3

Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota.

Wang J, Thingholm L B, Skiecevičienė J, Rausch P, Kummen M, Hov J R, Degenhardt F, Heinsen F A, Rühlemann M C, Szymczak S, Holm K, Esko T, Sun J, Pricop-Jeckstadt M, Al-Dury S, Bohov P, Bethune J, Sommer F, Ellinghaus D, Berge R K, Hübenthal M, Koch M, Schwarz K, Rimbach G, Hübbe P, Pan W H, Sheibani-Tezerji R, Häsler R, Rosenstiel P, D’Amato M, Cloppenborg-Schmidt K, Künzel S, Laudes M, Marschall H U, Lieb W, Nöthlings U, Karlsen T H, Baines J F, Franke A (2016); Nat Genet., 48(11):1396-1406. doi: 10.1038/ng.3695

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