The evolutionary origin of animal cellulose synthase

Abstract

Urochordates are the only animals that produce cellulose, a polysaccharide existing primarily in the extracellular matrices of plant, algal, and bacterial cells. Here we report a Ciona intestinalis homolog of cellulose synthase, which is the core catalytic subunit of multi-enzyme complexes where cellulose biosynthesis occurs. The Ciona cellulose synthase gene, Ci-CesA, is a fusion of a cellulose synthase domain and a cellulase (cellulose-hydrolyzing enzyme) domain. Both the domains have no animal homologs in public databases. Exploiting this fusion of atypical genes, we provided evidence of a likely lateral transfer of a bacterial cellulose synthase gene into the urochordate lineage. According to fossil records, this likely lateral acquisition of the cellulose synthase gene may have occurred in the last common ancestor of extant urochordates more than 530 million years ago. Whole-mount in situ hybridization analysis revealed the expression of Ci-CesA in C. intestinalis embryos, and the expression pattern of Ci-CesA was spatiotemporally consistent with observed cellulose synthesis in vivo. We propose here that urochordates may use a laterally acquired "homologous" gene for an analogous process of cellulose synthesis.