B1
Recognition and Communication

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

We live in a symbiotic world. All metaorganisms alike must have mechanisms in place to discriminate between microorganisms and to establish bacterial colonization during host development. However, the factors that are influencing the processes remain poorly understood.

In the first funding phase, the project of PI Hentschel (B1.1) focused on describing differential sponge responses to microorganisms by using an experimental approach in combination with transcriptome sequencing. Additionally, an experimentally tractable model for sponge symbioses was developed. In the project of PI Fraune (B1.2), co-occurrence networks indicated that bacterial interactions are dynamic throughout Nematostella development and certain competitive bacteria were shown to influence community structure over time. Re-colonization experiments indicated on one hand that bacteria-bacteria interactions are essential factors controlling colonization dynamics, while on the other hand RNA-Seq experiments indicated that the host might be involved in shaping initial colonization events.

In the second funding phase, we will build on these results and focus our efforts on two overarching aims:

(i) Do host mechanisms, especially phagocytosis, control bacterial colonization events in early branching metazoan taxa?
(ii) Which role do bacteria-bacteria interactions play in the assembly of the microbiome?

The new insights, which will be derived from in vitro and in vivo studies in both model systems, will unveil possibly ancient mechanisms of host-microbe cross talk and will provide insights into the patterns and successions that shape microbial colonization dynamics. As sponges and cnidaria preserved much of the genetic complexity of the common metazoan ancestor, our project promises to discover conserved mediators, which have evolved early in evolution as controls of bacterial colonization.

By combining our highly complementary expertise with respect to animal models and microbiology, we will be in a unique position to identify general rules of host-microbe and microbe-microbe interactions of which some may be conserved across all animal life while others may be unique to specific animal groups.

B1
Researchers

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B1.1: Mechanistic and cellular underpinnings of sponge-microbe cross talk

B1.2: Mechanisms determining temporal bacterial colonization dynamics during Nematostella development

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Related Publications

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2023
B1

Maternal provisioning of an obligate symbiont

Carrier TJ, Schmittmann L, Jung S, Pita L, Hentschel U. Maternal provisioning of an obligate symbiont in a sponge. Ecology and Evolution. 2023; 13: e10012  DOI: 10.1002/ece3.10012
2023
B1

A novel in-vivo phagocytosis assay to gain cellular insights on sponge-microbe interactions

Angela M. Marulanda-GomezK Kristina BayerLucia PitaUte Hentschel (2023)
2023
A1
B1
INF
Z2

Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis

Domin H, Zimmermann J, Taubenheim J, Fuentes Reyes G, Saueressig L, Prasse D, Höppner M, Schmitz RA, Hentschel U, Kaleta C, Fraune S (2023) Sequential host-bacteria and bacteria-bacteria interactions determine the microbiome establishment of Nematostella vectensis. Microbiome doi:10.1186/s40168-023-01701-z

 

 

 

 

2022
B1
C4

Sponge-symbiont stability in spite of antibiotic-induced microbiome disturbance

Schmittmann L, Rahn T, Busch K, Fraune S, Pita L, Hentschel U. (2022)  Environ. Microbiol. 24: 6392-6410, https://doi.org/10.1111/1462-2920.16249

2022
B1

Harnessing the power of model organisms to unravel coral holobiont complexity

Puntin G., Sweet M, Fraune S., Medina M., Weiss V, Ziegler M (2022)  Microbiol. Mol. Biol. Reviews, 21;86(4):e0005322, https://doi.org/10.1128/mmbr.00053-22

2022
B1

Stability of a dominant sponge-symbiont in spite of antibiotic-induced microbiome disturbance

Schmittmann L, Rahn T, Busch K, Fraune S, Pita L, Hentschel U. Stability of a dominant sponge-symbiont in spite of antibiotic-induced microbiome disturbance (2022)  Environ. Microbiol. 24: 6392-6410, https://doi.org/10.1111/1462-2920.16249

2022
B1

Pigmentation biosynthesis influences the microbiome in sea urchins

Wessel Gary M. Kiyomoto Masato, Reitzel Adam M and Carrier Tyler J. (2022) in R. Soc. B. 289: 20221088 20221088 http://doi.org/10.1098/rspb.2022.1088

 

2022
B1.1
B1

Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome

Kathrin Busch, Beate M. Slaby, Wolfgang Bach, Antje Boetius, Ina Clefsen, Ana Colaço, Marie Creemers, Javier Cristobo, Luisa Federwisch, Andre Franke, Asimenia Gavriilidou, Andrea Hethke, Ellen Kenchington, Furu Mienis, Sadie Mills, Ana Riesgo, Pilar Ríos, Emyr Martyn Roberts, Detmer Sipkema, Lucía Pita, Peter J. Schupp, Joana Xavier, Hans Tore Rapp & Ute Hentschel (2022) Nature Communications. 13: 5160. doi: 1038/s41467-022-32684-4

2022
B1.2
B1

Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis

Laura Baldassarre, Hua Ying, Adam M. Reitzel, Sören Franzenburg, Sebastian Fraune (2022): Nature Communications, 13, Article number: 3804 doi: 10.1038/s41467-022-31350-z

2022
B1

On the spread of microbes that manipulate reproduction in marine invertebrates.

Kustra MC, Carrier TJ (2022)  The American Naturalist. 200(20):1-19. doi: 1086/720282

2022
B1
C1
C4

Symbiotic Algae of Hydra viridissima Play a Key Role in Maintaining Homeostatic Bacterial Colonization.

Bathia J, Schröder K, Fraune S, Lachnit T, Rosenstiel P, Bosch TCG (2022) Front. Microbiol. 13:869666. doi: 10.3389/fmicb.2022.869666

2022
B1
C1

Symbiont transmission in marine sponges: reproduction, development, and metamorphosis

Carrier TJ, Maldonado M, Schmittmann L, Pita L, Bosch TCG, Hentschel U (2022) BMC Biology 20(1):100 doi: 10.1186/s12915-022-01291-6

2022
B1
Z3

Population differences and host species predict variation in the diversity of host-associated microbes in Hydra

Taubenheim J, Miklós M, Tökölyi J, Fraune S (2022). Front. Microbiol. 13:799333. doi: 10.3389/fmicb.2022.799333

2022
B1
C1

The role of DNA methylation in genome defense in Cnidaria and other invertebrates

Ying H, Hayward DC, Klimovich A, Bosch TCG, Baldassarre L, Neeman T, Forêt S, Huttley G, Reitzel AM, Fraune S, Ball EE, Miller DJ (2022) Molecular Biology and Evolution, msac018, doi: 10.1093/molbev/msac018

2021
B1

Contribution of maternal and paternal transmission to bacterial colonization in Nematostella vectensis.

Baldassarre L, Levy S, Bar-Shalom R, Steindler L, Lotan T, Fraune S (2021)  Front Microbiol. 12: 726795. doi: 3389/fmicb.2021.726795

2021
B1
C4

Harnessing the power of host–microbe symbioses to address grand challenges.

Hentschel U (2021) Nat Rev Microbiol. 19, 615–616. doi: 10.1038/s41579-021-00619-3

2021
B1

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panacea

Schmittmann L, Franzenburg S, Pita L (2021)  Front Immunol. 12:689051. doi: 3389/fimmu.2021.689051.

2021
B1

Hydra and Curvibacter – an intimate crosstalk at the epithelial interface. In: Cellular Dialogues in the Holobiont.

Minten T, Fraune S (2021)  ed. by Bosch, Thomas C. G. and Hadfield, Michael G.. CRC Press, Boca Raton, Fla., USA, pp. 79-89 ISBN 9780429277375 doi: 1201/9780429277375-4.

2021
B1

Decoding cellular dialogues between sponges, bacteria, and phages. In: Cellular Dialogues in the Holobiont.

Schmittmann L, Jahn MT, Pita L, Hentschel U (2021) ed. by Bosch, Thomas C. G. and Hadfield, Michael G.. CRC Press, Boca Raton, Fla., USA, pp. 49-63. ISBN 9780429277375 doi: 1201/9780429277375-4.

2021
B1
C4

Lifestyle of sponge symbiont phages by host prediction and correlative microscopy

Jahn MT, Lachnit T, Markert SM, Stigloher C, Pita L, Ribes M, Dutilh BE, Hentschel U (2021) ISME J. doi: 10.1038/s41396-021-00900-6

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
B1

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

Rix L, Ribes M, Coma R, Jahn M, van Oevelen D, de Goeij J, Escrig S, Meibom A, Hentschel U (2020) ISME J. 14, 2554–2567. doi: 10.1038/s41396-020-0706-3

2020
A1
B1

Receptors mediating host-microbiota communication in the metaorganism: the invertebrate perspective.

Dierking K, Pita L (2020) Front. Immunol. 11:1251. doi: 10.3389/fimmu.2020.01251

2020
A4
B1

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

Johnke J, Fraune S, Bosch TCG, Hentschel U, Schulenburg H (2020) Microbial Ecology. 79: 252–257. doi: 10.1007/s00248-019-01395-7

2019
A4
B1
C2
C3

A 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

2019
A1
A2
A3
B1
B2
C1
C2
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
C1
C2

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
A2
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
A4
B1
B2

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

2019
B1
C3

Fueled 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
B1
INF
Z2

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

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
B1

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

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
A2
B1
INF
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
A1
A2
A3
A4
B1
B2
C1
C3
Z1

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
A4
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
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
B1
Z2

Emerging Sponge Models of Animal-Microbe Symbioses.

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

2016
B1
Z2

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

2016
A4
B1

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

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