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.

Transposon-mediated insertional mutagenesis revealed the functions of animal cellulose synthase in the ascidian Ciona intestinalis

“…It was unexpected that both larval and adult tunics were formed in sj mutants. Ci-CesA is the only gene encoding cellulose synthase in the C. intestinalis genome (4,6), and cellulose synthase plays a critical role in cellulose synthesis in plants and bacteria (26,27). Hence, it is expected that the loss of cellulose from the tunic of sj mutants would cause malformation of the tunic.…”

“…Cellulose synthase is an enzyme that has a central role in cellulose biosynthesis; the gene (Ci-CesA) for cellulose synthase is encoded in the Ciona intestinalis genome and expressed in the larval ectoderm (4). Recent molecular phylogenetic analyses of Ci-CesA and Cs-CesA of Ciona savignyi suggest that the gene has been acquired by horizontal transfer from bacteria (5,6). Ascidian cellulose synthase may be involved in the formation of the tunic, the cellulose-containing structure that surrounds the surface of the body to protect against predators.…”

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…The acquisition by the urochordate Ciona intestinalis of a cellulose synthase gene of cyanobacterial origin has been proposed [64]. This acquisition gives these animals the ability (unique among animals) of cellulose biosynthesis.…”

Chordate evolution and the three-phylum system

“…Two key enzymes for cellulose biosynthesis are cellulose synthase (CesA) and cellulase. The Ciona genome contains a single copy of CesA (Ci-CesA) [91,92]. Molecular phylogeny indicates that Ci-CesA is included within a clade of Streptomyces CesA, suggesting that the bacterial CesA gene probably jumped horizontally into the genome of a tunicate ancestor earlier than 550 Ma.…”