The pivotal role of cyanobacteria in the evolution of cellulose synthases and cellulose synthase-like proteins

Cellulose synthase and other members of the family 2 glycosyltransferases are ubiquitous in all kingdoms of life. To date, no attempt has been made to construct a phylogeny that positions cellulose synthases in relation to other members of this family or to elucidate relationships within the cellulose synthase group. In this study, a sequence from the unicellular, marine cyanobacterium Synechococcus sp. PCC 7002 is shown to share a unique common ancestor of a clade consisting of cellulose synthases from Dictyostelium dis­ coideum and Nostoc, as well as a plant grouping that includes CesA proteins and cellulose synthase-like (CsI) proteins G, E, B, D, and F. A branching order is established for Csi proteins that places CsIG as ancestral to other members of the CsI/CesA clade. Sequences from Ciona intestinalis and Aspergillis fu­ migatus are shown to branch at the base of the Eukaryota/Cyanobacteria clade. These data suggest multiple independent transfers of cellulose synthases. The implications of these findings in relation to the evolu­ tionary history of cellulose synthase are discussed. Introduction Cellulose synthases and related enzymes chitin synthases, Class I and II hyaluronan synthases Cellulose is the most abundant biopolymer on (HAS), Nod C proteins, and plant cellulose syn­ earth with some lOll tons produced annually thase-like (Csl) proteins are processive fi-glyco­ (Hess et al. 1928). The biosynthesis of cellulose has syltransferases (PGBTs), belonging to the family 2 been demonstrated in a number of prokaryotes, glycosyltransferases. These enzymes are integral including members of the Cf. and}' Proteobacteria membrane proteins with multiple transmembrane (Ross et al. 1991; Zogaj et al. 2001), Finnicutes domains, sharing the conserved D,D,D,QXXRW (Roberts 1991), and sections I, III, and IV of the residues within a cytosolic catalytic region (Saxena cyanobacteria (Nobles et al. 2001). Among et al. 1995; Saxena and Brown 2000). The uni­ eukaryotic organisms, cellulose biosynthesis has versal presence of this motif is consistent with been observed in animals (tunicates), algae, vas­ origination from a common ancestral protein. cular plants such as mosses and ferns, gymno­ Recent availability of complete and incomplete sperms and angiosperms (Brown 1985), the genome sequences has led to an increase in the cellular slime mold Dictyostelium discoideum number of known sequences that, based on the (Blanton et al. 2000), and in the free-living amoeba presence of the D,D,D,QXXRW motif, are pre­ Acanthamoeba spp. (Linder et a1. 2002). dicted to encode PGBTs. In fact, available