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.
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
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
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
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
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
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
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