Bacteria- and temperature-regulated peptides modulate β-catenin signaling in
            <i>Hydra</i>

Taubenheim, Jan; Willoweit-Ohl, Doris; Knop, Mirjam; Franzenburg, Sören; He, Jinru; Bosch, Thomas C. G.; Fraune, Sebastian

doi:10.1073/pnas.2010945117

Cited by 18 publications

(15 citation statements)

References 88 publications

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“…7 g). We assume that this task is especially important when beta-Catenin/TCF levels are increased, which may occur in Hydra under natural conditions, for example in interaction with the environment [ 52 ], or as a response to injury [ 38 ].…”

Section: Resultsmentioning

confidence: 99%

The Wnt-specific astacin proteinase HAS-7 restricts head organizer formation in Hydra

et al. 2021

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Background The Hydra head organizer acts as a signaling center that initiates and maintains the primary body axis in steady state polyps and during budding or regeneration. Wnt/beta-Catenin signaling functions as a primary cue controlling this process, but how Wnt ligand activity is locally restricted at the protein level is poorly understood. Here we report a proteomic analysis of Hydra head tissue leading to the identification of an astacin family proteinase as a Wnt processing factor. Results Hydra astacin-7 (HAS-7) is expressed from gland cells as an apical-distal gradient in the body column, peaking close beneath the tentacle zone. HAS-7 siRNA knockdown abrogates HyWnt3 proteolysis in the head tissue and induces a robust double axis phenotype, which is rescued by simultaneous HyWnt3 knockdown. Accordingly, double axes are also observed in conditions of increased Wnt activity as in transgenic actin::HyWnt3 and HyDkk1/2/4 siRNA treated animals. HyWnt3-induced double axes in Xenopus embryos could be rescued by coinjection of HAS-7 mRNA. Mathematical modelling combined with experimental promotor analysis indicate an indirect regulation of HAS-7 by beta-Catenin, expanding the classical Turing-type activator-inhibitor model. Conclusions We show the astacin family protease HAS-7 maintains a single head organizer through proteolysis of HyWnt3. Our data suggest a negative regulatory function of Wnt processing astacin proteinases in the global patterning of the oral-aboral axis in Hydra.

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Section: Resultsmentioning

confidence: 99%

The Wnt-specific astacin proteinase HAS-7 restricts head organizer formation in Hydra

et al. 2021

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“…However, even if the species differences were small, they might still be functionally important. For instance, in laboratory experiments with Hydra , single bacterial taxa can provide important fitness benefits to the host ( Fraune et al, 2015 ; Taubenheim et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

“…Animals with their microbiota experimentally removed have reduced movement and contractility ( Murillo-Rincon et al, 2017 ) and impaired ability to reproduce asexually ( Rahat and Dimentman, 1982 ). Interactions between microbial components influence pattern formation ( Taubenheim et al, 2020 ), and can induce tumor development ( Rathje et al, 2020 ), but the presence of core microbial elements also protects the host against fungal infections ( Fraune et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

Population Differences and Host Species Predict Variation in the Diversity of Host-Associated Microbes in Hydra

et al. 2022

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Most animals co-exist with diverse host-associated microbial organisms that often form complex communities varying between individuals, habitats, species and higher taxonomic levels. Factors driving variation in the diversity of host-associated microbes are complex and still poorly understood. Here, we describe the bacterial composition of field-collected Hydra, a freshwater cnidarian that forms stable associations with microbial species in the laboratory and displays complex interactions with components of the microbiota. We sampled Hydra polyps from 21 Central European water bodies and identified bacterial taxa through 16S rRNA sequencing. We asked whether diversity and taxonomic composition of host-associated bacteria depends on sampling location, habitat type, host species or host reproductive mode (sexual vs. asexual). Bacterial diversity was most strongly explained by sampling location, suggesting that the source environment plays an important role in the assembly of bacterial communities associated with Hydra polyps. We also found significant differences between host species in their bacterial composition that partly mirrored variations observed in lab strains. Furthermore, we detected a minor effect of host reproductive mode on bacterial diversity. Overall, our results suggest that extrinsic (habitat identity) factors predict the diversity of host-associated bacterial communities more strongly than intrinsic (species identity) factors, however, only a combination of both factors determines microbiota composition in Hydra.

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“…There are intricate interactions between the nervous system of Hydra and its associated microbiome ( Augustin et al, 2017 ; Murillo-Rincon et al, 2017 ). and we have shown that the microbiome controls developmental programs via Wnt ( Taubenheim et al, 2020 ). It thus seems that the cnidarian nervous system is able to integrate environmental signals, like the associated bacteria, into developmental pathways.…”

Section: From Environmental Sensor To Developmental Determinantmentioning

confidence: 99%

Function and Evolution of Nuclear Receptors in Environmental-Dependent Postembryonic Development

Taubenheim

Kortmann

Fraune

2021

Front. Cell Dev. Biol.

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Nuclear receptors (NRs) fulfill key roles in the coordination of postembryonal developmental transitions in animal species. They control the metamorphosis and sexual maturation in virtually all animals and by that the two main environmental-dependent developmental decision points. Sexual maturation and metamorphosis are controlled by steroid receptors and thyroid receptors, respectively in vertebrates, while both processes are orchestrated by the ecdysone receptor (EcR) in insects. The regulation of these processes depends on environmental factors like nutrition, temperature, or photoperiods and by that NRs form evolutionary conserved mediators of phenotypic plasticity. While the mechanism of action for metamorphosis and sexual maturation are well studied in model organisms, the evolution of these systems is not entirely understood and requires further investigation. We here review the current knowledge of NR involvement in metamorphosis and sexual maturation across the animal tree of life with special attention to environmental integration and evolution of the signaling mechanism. Furthermore, we compare commonalities and differences of the different signaling systems. Finally, we identify key gaps in our knowledge of NR evolution, which, if sufficiently investigated, would lead to an importantly improved understanding of the evolution of complex signaling systems, the evolution of life history decision points, and, ultimately, speciation events in the metazoan kingdom.

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Bacteria- and temperature-regulated peptides modulate β-catenin signaling in Hydra

Cited by 18 publications

References 88 publications

The Wnt-specific astacin proteinase HAS-7 restricts head organizer formation in Hydra

The Wnt-specific astacin proteinase HAS-7 restricts head organizer formation in Hydra

Population Differences and Host Species Predict Variation in the Diversity of Host-Associated Microbes in Hydra

Function and Evolution of Nuclear Receptors in Environmental-Dependent Postembryonic Development

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