C1

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

Inter-species interactions in the freshwater polyp Hydra between symbiotic algae and host cells had been the subject of research since decades since they not only provide insights into the basic “tool kit” necessary to establish symbiotic interactions, but are also of relevance in understanding the resulting evolutionary selection processes. A long term persistence of symbiotic associations is prevalent not only in two-party interactions of Hydra and symbiotic algae, but also in more complex systems including stable associated bacteria. Studying symbiotic inter-species interactions in Hydra, therefore, may be a paradigmatic example of a complex symbiotic community that influences the host´s health and development. Starting from one of “the” classical model systems in developmental biology, we used Hydra in the last few years to explore host-microbe interactions. Our findings reveal that epithelia and components of the innate immune system play an active role in selecting the inhabitant microbiota via a complex genetic network. The work has contributed to a paradigm shift in evolutionary immunology:

Components of the innate immune system with its host-specific antimicrobial peptides appear to have evolved in early branching metazoans because of the need to control the resident beneficial microbes rather than because of invasive pathogens. Yet in spite of all these insights in an ultimately simple metaorganism we have still not been able to coherently integrate the accumulated abundance of information into a truly mechanistic understanding of host-microbe interactions. To understand common principles of symbiogenesis and their links to metaorganism evolution, we examine the impact of symbiotic microbes and algae on developmental processes in Hydra.

Elucidating these issues will not only contribute to our understanding of the genetic basis of microbial speciation and adaptation within eukaryotic hosts but will also provide conceptual insights into the impact of beneficial microbes on the host life history and the complexity of host-microbe interactions in general.

Researchers

Jay Bathia

PhD Candidate
Kiel University Zoological Institute

Jinru He

PhD Candidate
Kiel University Zoological Institute

Alumni

Publications

2020

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 Pathogen. 16(3):e1008375. doi: 10.1371/journal.ppat.1008375

2019

FeaturedAdvancing 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

 

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

FeaturedTemperature 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

FeaturedTransgenesis 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

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

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

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

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

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

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

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

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

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

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

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

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

FeaturedA 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

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

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