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Function and Life History

Towards understanding an ultimately simple metaorganism: impact of symbiotic microbes and algae on developmental processes of Hydra and their adaption within the host

Animal developmental programs occur within the context of coevolved associations with microbes. Hydra is one of the prime model systems for evolutionary developmental biologists. The fact that symbiotic interactions were discovered to be essential to development in numerous animals, lead us to propose using Hydra to uncover the common principles of symbiogenesis and their links to evolution with particular emphasis on developmental programs. Our prior work has shown that the epithelial surface is densely colonized by a stable multi-species bacterial community. Each Hydra species supports long-term associations with a different set of bacteria. Hydra host shapes the specific microbiome by means of the innate immune system and a rich repertoire of antimicrobial peptides.

In the first funding period (C1.1, PI Bosch) we established a long-term germ-free Hydra culture and discovered that (i) the presence and structure of this microbiota is critical not only for the health of the polyps but also for patterning processes and tissue homeostasis; (ii) the transcription factor FoxO provides a direct link between stem cell proliferation, tissue homeostasis, and the microbiota; and (iii) there is a direct interaction between neurons and microbes.

In the second funding period we will expand on the past findings to address two specific questions:

(i) How do resident microbiota affect developmental and patterning processes in adult Hydra polyps? Answering this question relies on large-scale unbiased and systematic identification of bacteria-responsive patterning-associated Hydra genes using comparative transcriptomic analysis (RNAseq) followed by their functional analysis.

(ii) Do microbes play a role in Hydra´s early embryonic development? And more specifically, do resident microbiota influence neurogenesis in embryos and/or in adults? Is the resident microbiota involved in educating neuronal precursor cells/stem cells which, in turn, influence the composition of the microbiota? This question is based on preliminary observations of polyps with abnormal morphology hatching from eggs produced by germ-free females.

Our newly established mass-culture of long-term germ-free animals in combination with the well-equipped tool box for studying Hydra development and the expertise of the CRC consortium in analysing and modelling interactions between microbes and evolving metaorganisms will allow to find answers to these questions. Elucidating these issues will not only contribute to the understanding of host interactions with microbial communities in one of the simplest possible animal systems but may also provide conceptual insights into the complexity of host-microbe interactions in general. The project will assist our understanding of how all of the parts of a living organism operate together within a meta-organismic framework.

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2020
B1
C1

Bacteria- and temperature-regulated peptides modulate beta-catenin signalling in Hydra

Taubenheim J, Willoweit-Ohl D, Knop M, Franzenburg S, He J, Bosch TCG, Fraune S (2020) PNAS. 117(35):21459-21468. doi: 10.1073/pnas.2010945117

2020
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Exploring the niche concept in a simple metaorganism

Deines P, Hammerschmidt K, TCG Bosch (2020) Frontiers in Microbiology, 11:1942, 1-11. doi: 10.3389/fmicb.2020.01942 

2020
C1

Microbial species coexistence depends on the host environment

Deines P, Hammerschmidt K, Bosch TCG (2020) mBio 11:e00807-20. doi: 10.1128/mBio.00807-20.

2020
C1

Prototypical pacemaker neurons interact with the resident microbiota

Klimovich A, Giacomello S, Björklund Å, Faure L, Kaucka M, Giez C, Murillo-Rincon AP, Matt A, Willoweit-Ohl D, Crupi G, de Anda J, Wong GCL, D’Amato M, Adameyko I, Bosch TCG (2020) PNAS. 117 (30) 17854-17863. doi: 10.1073/pnas.1920469117

2020
C1
INF

Dynamic interactions within the host-associated microbiota cause tumor formation in the basal metazoan Hydra.

Rathje K, Mortzfeld B, Hoeppner MP, Taubenheim J, Bosch TCG, Klimovich A (2020) PLoS Pathog. 16(3):e1008375. doi: 10.1371/journal.ppat.1008375

2020
C1

Are noncommunicable diseases communicable?

Finlay BB,  Blaser MJ, Bosch TCG, Dominguez-Bello MG, Elinav E, McFall-Ngai M, Melby MK, Muehlmann SR,  Sansonetti PJ (2020) Science. 367(6475): 250-251. doi: 10.1126/science.aaz3834 

2019
A3
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INF

Advancing our functional understanding of host–microbiota interactions: a need for new types of studies

He J, Lange J, Marinos G, Bathia J, Harris D, Soluch R, Vaibhvi V, Deines P, Hassani MA, Wagner K-S, Zapien‐Campos R, Jaspers C, Sommer F (2019) BioEssays, 1900211 (1-5). doi: 10.1002/bies.201900211

 

2019
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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
A4
B1
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Temperature and insulin signaling regulate body size in Hydra by the Wnt and TGF-beta pathways

Mortzfeld BM*, Taubenheim J*, Klimovich AV, Fraune S, Rosenstiel P, Bosch TCG (2019) Nature Communications 10, 3257. doi: 10.1038/s41467-019-11136-6

2019
C1

Transgenesis in Hydra to characterize gene function and visualize cell behaviour.

Klimovich A, Wittlieb J, Bosch TCG (2019) Nat. Protoc., 1-24. doi: 10.1038/s41596-019-0173-3

2019
A4
C1

The microbiome mediates environmental effects on ageing

Finlay B, Pettersson S, Melby M, Bosch TCG (2019) BioEssays, 1800257, 1-7; doi: 10.1002/bies.201800257

2019
A4
C1

Evolutionary “experiments” in symbiosis: the study of model animals provides insights into the mechanisms underlying diversity of host-microbe interactions

Bosch TCG, Guillemin K, McFall-Ngai M (2019) BioEssays, 1800256 (1-8). doi: 10.1002/bies.201800256

2018
A2
B2
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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
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C1
Z1

Hydra as Model to Determine the Role of FOXO in Longevity

Bosch TCG (2018); Methods Mol Biol. 1890:231-238. doi: 10.1007/978-1-4939-8900-3_19

2018
A4
B1
C1
Z1

Metabolic co-dependence drives the evolutionarily ancient Hydra-Chlorella symbiosis.

Hamada M, Schröder K, Bathia J, Kürn U, Fraune S, Khalturina M, Khalturin K, Shinzato C, Satoh N, Bosch TC (2018); Elife 7. pii: e35122. doi: 10.7554/eLife.35122

2018
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C1
C2
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Grow With the Challenge – Microbial Effects on Epithelial Proliferation, Carcinogenesis, and Cancer Therapy

Von Frieling J, Fink C, Hamm J, Klischies K, Forster M, Thomas C. G. Bosch TCG, Roeder T, P Rosenstiel P, Sommer F (2018); Front. Microbiol. doi: 10.3389/fmicb.2018.02020

2018
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C1
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Non-senescent Hydra tolerates severe disturbances in the nuclear lamina.

Klimovich A, Rehm A, Wittlieb J, Herbst EM, Benavente R, Bosch TCG (2018); Aging (Albany NY) 10(5):951-972. doi: 10.18632/aging.101440

2018
A4
C1
Z1

Rethinking the Role of the Nervous System: Lessons From the Hydra Holobiont.

Klimovich AV, Bosch TCG (2018); Bioessays 40(9):e1800060. doi: 10.1002/bies.201800060

2018
A4
B1
C1
Z1

Stem cell transcription factor FoxO controls microbiome resilience in Hydra.

Mortzfeld B M, Taubenheim J,Fraune S, Klimovich A V, Bosch T C G (2018); Front Microbiol., doi: 10.3389/fmicb.2018.00629

2018
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C3
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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

2018
A4
C1
Z1

How the microbiome challenges our concept of self.

Rees T, Bosch T G C, Douglas A E (2018); PloS Biol., 16(2):e2005358. doi:10.1371/journal.pbio.2005358

2017
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B1
C1
Z1

Temperate phages as self-replicating weapons in bacterial competition.

Li XY, Lachnit T, Fraune S, Bosch T C G, Traulsen A, Sieber M (2017); J R Soc Interface, 14(137). doi: 10.1098/rsif.2017.0563

2017
A4
C1
Z1

Spontaneous body contractions are modulated by the microbiome of Hydra.

Murillo-Rincon A P, Klimovich A, Pemöller E, Taubenheim J, Mortzfeld B, Augustin R, Bosch T C G (2017); Scientific Reports, 7(15937). doi:10.1038/s41598-017-16191-x

2017
A4
B1
C1
Z1

A secreted antibacterial neuropeptide shapes the microbiome of Hydra.

Augustin R, Schröder K, Murillo Rincón A P, Fraune S, Anton-Erxleben F, Herbst E M, Wittlieb J, Schwentner M, Grötzinger J, Wassenaar T M, Bosch T C G (2017); Nat Commun., 8(1):698. doi: 10.1038/s41467-017-00625-1

2016
A4
C1
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The Origin of Mucosal Immunity: Lessons from the Holobiont Hydra.

Schröder K, Bosch T C (2016); MBio., 7(6):e01184-16. doi: 10.1128/mBio.01184-16

2016
A4
C1
Z1

Transitioning from Microbiome Composition to Microbial Community Interactions: The Potential of the Metaorganism Hydra as an Experimental Model.

Deines P, Bosch T C G (2016); Front. Microbiol., 7:1610. doi: 10.3389/fmicb.2016.01610

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