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

Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21459-21468. doi: 10.1073/pnas.2010945117. Epub 2020 Aug 19.

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, and we used it here 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, germfree 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 up-regulated 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.

Keywords: Eco-Evo-Devo; Wnt signaling; host–microbe interaction; orphan gene; phenotypic plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteria / metabolism
  • Body Patterning / genetics
  • Gene Expression Regulation, Developmental / genetics
  • Gene-Environment Interaction
  • Hydra / genetics*
  • Hydra / metabolism*
  • Hydra / physiology
  • Peptides / metabolism
  • Temperature
  • Wnt Proteins / metabolism
  • Wnt Signaling Pathway / genetics
  • Wnt Signaling Pathway / physiology
  • beta Catenin / metabolism*

Substances

  • Peptides
  • Wnt Proteins
  • beta Catenin