B1

Host-microbe cross talk in the early metazoan taxa Porifera and anthozoan Cnidaria

The term “metaorganism” was coined in recognition of the fact that in the environment, all multicellular hosts (animals, plants) associate with microorganisms. The concept has profound impacts on our understanding of ecology which seeks to understand the interactions between organisms and between organisms and their environment. There is a growing awareness that such microbial communities may fulfill many essential functions, from nutrition to development and defense against pathogens.

This proposal B1 seeks to investigate host-microbe interactions in two early-branching metazoans, sponges and cnidarians. It was shown that sponges and cnidarians are colonized by specific bacterial communities, which is suggestive of highly selective pressures by the host animal. Recent genome projects of sponges and cnidarians have identified potential receptors, signal transduction cascades, and effector molecules involved in epithelial defence. In this proposal, we hypothesize that there is an intimate interaction between bacterial community and the host immune system and that the bacterial colonizers will contribute to host fitness. Neither aspect has been investigated in detail in the proposed experimental models. To elucidate these interactions, we will focus on two main aims in Nematostella and two selected sponge species in a comparative approach:
1. Host mechanisms involved in recognition and establishment of specific bacterial colonization.
2. Bacterial function and localization during development.

Together, these insights, which will be derived from in vitro and in vivo studies, will unveil ancient mechanisms controlling host-microbe recognition, function and homeostasis during development. Because these phyla have preserved much of the genetic complexity of the common metazoan ancestor it promises to be highly informative to discover evolutionarily conserved mechanisms controlling host-microbe interactions.

Researchers

Martin T. Jahn

PhD Candidate
GEOMAR - Helmholtz Centre for Ocean Research Kiel

Hanna Domin

Associated Researcher
Heinrich-Heine Universität Düsseldorf

Dr. Anna Roik

Associated Researcher
Kiel University Institute for General Microbiology

Lara Schmittmann

Associated Researcher
GEOMAR - Helmholtz Centre for Ocean Research Kiel

Publications

2019

FeaturedA phage protein aids bacterial symbionts in eukaryote immune evasion

Jahn MT, Arkhipova K, Markert SM, Stigloher C, Lachnit T, Pita L, Kupczok A, Ribes M, Stengel ST, Rosenstiel P, Dutilh BE, Hentschel U (2019) Cell Host & Microbe, doi: 10.1016/j.chom.2019.08.019

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

FeaturedNeutrality 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

Bdellovibrio and like organisms are predictors of microbiome diversity across diverse host groups.

Johnke J, Fraune S, Bosch TCG, Hentschel U, Schulenburg H (2019) Microbial Ecology DOI: 10.1007/s00248-019-01395-7

Resolving structure and function of metaorganisms through a holistic framework 2 combining reductionist and integrative approaches

Jaspers C, Fraune S, Consortium of Australian Academy of Science Boden Research Conference Participants, Arnold AE, Miller DJ, Bosch TCG, Voolstra CR (2019) Zoology. doi: 10.1016/j.zool.2019.02.007

FeaturedFueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts

Rubin-Blum M, Antony CP, Sayavedra L, Martínez-Pérez C, Birgel D, Peckmann J, Wu Y, Cardenas P, MacDonald I, Marcon Y, Sahling H, Hentschel U, Dubilier N (2019) The ISME Journal , v 13, p 1209–1225. doi: 10.1038/s41396-019-0346-7

2018

Differential expression of immune receptors in two marine sponges upon exposure to microbial-associated molecular patterns.

Pita L, Hoeppner MP, Ribes M, Hentschel U (2018); Sci Rep. 8(1):16081.doi: 10.1038/s41598-018-34330-w

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

Predicted bacterial interactions affect in vivo microbial colonization dynamics in Nematostella

Domin H, Zurita-Gutiérrez Y, Scotti M, Buttlar J, Hentschel Humeida U and Fraune S  (2018) Frontiers in Microbiology 9, 728, https://doi.org/10.3389/fmicb.2018.00728

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

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

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

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

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

Emerging Sponge Models of Animal-Microbe Symbioses.

Pita L, Fraune S, Hentschel U (2016); Front Microbiol., 7:2102. doi: 10.3389/fmicb.2016.02102

Shedding light on cell compartmentation in the candidate phylum Poribacteria by high resolution visualisation and transcriptional profiling.

Jahn M T, Markert S M, Ryu T, Ravasi T, Stigloher C, U Hentschel, Moitinho-Silva L (2016); Scientific Reports, 6:35860. doi: 10.1038/srep35860

Using Nematostella vectensis to Study the Interactions between Genome, Epigenome, and Bacteria in a Changing Environment.

Fraune S, Forêt S, Reitzel A M (2016); Front. Mar. Sci., 3:148. doi: 10.3389/fmars.2016.00148