Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues

TLDR

The cellular microenvironment’s role in enabling metazoan tissue genesis is poorly understood, and the early‑branching ctenophora provide a unique model to investigate this evolutionary question. We examined the extracellular matrix of non‑bilaterian animal phyla, concentrating on collagen IV and spongin short‑chain collagens. We found that ctenophora possess basement membrane and collagen IV with structural and genomic features homologous to other non‑bilaterians and bilaterians, yet exhibit greater diversity with up to twenty collagen IV genes, whereas unicellular relatives lack collagen IV, supporting the view that collagen IV and spongin are primordial ECM components that facilitate the assembly of a basic architectural unit for multicellular tissue genesis.

Abstract

The role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Here, we characterized the extracellular matrix (ECM), with a focus on collagen IV and its variant, spongin short-chain collagens, of non-bilaterian animal phyla. We identified basement membrane (BM) and collagen IV in Ctenophora, and show that the structural and genomic features of collagen IV are homologous to those of non-bilaterian animal phyla and Bilateria. Yet, ctenophore features are more diverse and distinct, expressing up to twenty genes compared to six in vertebrates. Moreover, collagen IV is absent in unicellular sister-groups. Collectively, we conclude that collagen IV and its variant, spongin, are primordial components of the extracellular microenvironment, and as a component of BM, collagen IV enabled the assembly of a fundamental architectural unit for multicellular tissue genesis.