Bacteria- and temperature-regulated peptides modulate beta-catenin signaling inHydra

Abstract

Animal development has traditionally been viewed as an autonomous process directed by the host genome. But in many animals biotic and abiotic cues, like temperature and bacterial colonizers, provide signals for multiple developmental steps. Hydra offers unique features to encode these complex interactions of developmental processes with biotic and abiotic factors. Here, we used the model animal Hydra to investigate the impact of bacterial colonizers and temperature on the pattern formation process. In Hydra, formation of the head organizer involves the canonical Wnt pathway. Treatment with alsterpaullone (ALP) results in acquiring characteristics of the head organizer in the body column. Intriguingly, germ-free Hydra polyps are significantly more sensitive to ALP compared to control polyps. In addition to microbes, β -catenin dependent pattern formation is also affected by temperature. Gene expression analyses led to the identification of two small secreted peptides, named Eco1 and Eco2, being upregulated in the response to both, Curvibacter sp, the main bacterial colonizer of Hydra, and low temperatures. Loss-of function experiments revealed that Eco peptides are involved in the regulation of pattern formation and have an antagonistic function to Wnt signaling in Hydra. Our results in an early branching metazoan suggest that the Wnt pathway evolved as a signaling hub integrating environmental signals, like bacterial signals and temperature, into developmental processes and stem cell behavior.

Two separate but interconnected pattern formation systems are required to control body-axis and head-organiser formation inHydra

“…Furthermore, β -Catenin expression levels have been recently linked to ECM elasticity [100], which in turn plays an important chemical and mechanical role during pattern formation and regeneration. It has been also recently shown that even external biotic or abiotic environmental cues affect β -Catenin mediated signaling and pattern formation [12, 90]. In the light of the complexity of β -catenin/Tcf-related processes, it is rather likely that β -catenin-dependent HyWnt3 expression is only one of several pattern formation loops activated by gene expression downstream of β -catenin/Tcf [72, 104], thus making HyWnt3 expression dispensable for body axis formation.…”

“…Thus, it seems to be unlikely that the head organizer formation solely depends on β -catenin/Tcf activity considering the variety of extrinsic and intrinsic factors modulating β -catenin/Tcf levels in Hydra , e.g. [12, 36, 44, 77, 90, 100].…”

“…It is therefore unlikely that formation of the head organizer depends solely on β-catenin/Tcf activity, considering the variety of extrinsic and intrinsic factors modulating β-catenin/Tcf levels in Hydra, e.g. [12,37,45,79,91,102]. Based on the above considerations, we formulated a new mathematical model of symmetry breaking and pattern formation in Hydra, which could reproduce the dynamics of β-catenin/Tcf and Wnt3 activities.…”

A Wnt-specific astacin proteinase controls head formation inHydra

“…In particular, the dominance of a single organizer is ensured by HAS-7-driven degradation of the canonical Wnt ligands. 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 [37], or as a response to injury [29].…”

Oligonucleotide Library Assisted Sequence Mining Reveals Promoter Sequences With Distinct Temporal Expression Dynamics For Applications InCurvibactersp. AEP1-3

“…AEP1-3 (hereafter Curvibacter) is a rod-shaped ß-proteobacterial species best known for its symbiotic interaction with Hydra vulgaris [1], a freshwater polyp of the basal metazoan family Cnidaria, a sister group to the Bilateria. Together with other members of Hydras microbiota, they form a complex system of bacteria-bacteria as well as bacteria-host interactions [2,3,4]. While the host provides an ecological niche to its colonizers, the microbiota affects mobility, asexual reproduction as well as protection against fungi [1].…”