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Cellulose Production and the Evolution of the Sessile Lifestyle In Sessile Organisms 35（2）： 21–29（2018） The Sessile Organisms 総説/Review Society of Japan DOI: 10.4282/sosj.35.21 Cellulose production and the evolution of the sessile lifestyle in ascidians Yasunori Sasakura* Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka 415–0025, Japan * Corresponding author: Yasunori Sasakura E-mail: [email protected] (Received April 24, 2018; Accepted June 1, 2018; Published Online July 31, 2018) Abstract The outstanding characteristics of the marine invertebrate chordates, ascidians, are a sessile adult stage and cellulose production. These characteristics are not seen in other chordate groups. Molecular studies have suggested that these two characteristics are tightly linked. Ascidians possess the gene encoding cellulose synthase in their genomes. The disruption of the cellulose synthase gene results in abnormal metamorphosis and failure in adhesion, suggesting that cellulose is neces- sary for starting and continuing sessile life. Ascidian cellulose synthase is suspected to have been transferred to the tunicate ancestor from a bacterial group by horizontal gene transfer. It was suggested that by this transfer, the ancestor of tunicates was given both the gene body and an epidermal enhancer from the bacterium. The simultaneous transfer of these two ge- netic elements is thought to have facilitated the success of the gene transfer, which enabled the ancestor to utilize cellulose for evolving sessile ascidians. Keywords: tunicate, ascidian, Ciona, cellulose, metamorphosis, horizontal gene transfer Introduction ascidians. The overall morphology of adult ascidians is quite The phylum (or superphylum) Chordata (Fig. 1a) consists distinct from that of the typical tadpole structure, which is the of three groups: cephalochordates, tunicates, and vertebrates representative shape of chordates, and ascidians were previ- (Satoh et al., 2014). Among these groups, the cephalochordate ously misclassified with a different animal group (Satoh, group is at the most basal position according to the phyloge- 2003). netic analyses, and the tunicate and vertebrate groups form The chordate features of ascidians can be easily seen in sister groups with each other (Delsuc et al., 2006). Animals their larval body. The ascidian larva, unlike ascidian adult, ex- classified into the phylum chordate share some outstanding hibits the typical tadpole shape (Fig. 1c). The larva has a rod- characteristics that can be used to distinguish them from other like body with a thicker trunk and a long and thinner tail. The animal groups. For example, chordates have a notochord at tail includes a notochord at the center, surrounded by muscles a certain period of their life and a tubular central nervous that have striated muscle fibers. The larval CNS is located at system (CNS) at the dorsal part of the body. Most chordates the dorsal side. The CNS is formed by closure of the neural are free-living animals; they have developed muscle and are tube, which is a characteristic morphogenetic movement that motile at both their larval and adult stages. These characteris- is also seen in other chordates for the formation of a tubular tics enable us to recognize a chordate species relatively easily, CNS (Nicol and Meinertzhagen, 1988; Ogura et al., 2011). except for ascidians whose adults are difficult to be viewed as The thickened anterior side of the ascidian larval CNS is due chordates or even as animals. to the gathering of neurons to form the sensory vesicle that is Tunicates include thaliaceans and larvaceans in addition comparable to the brain of vertebrates (Wada et al., 1998; Du- to ascidians, and ascidians form the largest group among the four et al., 2006; Ikuta and Saiga, 2007). The CNS of the as- tunicates. Adult ascidians generally have a vase-like shape cidian larva includes motor neurons that regulate the contrac- (Fig. 1b), and they are immotile, sessile animals. The ses- tility of tail muscles for swimming (Horie et al., 2010; Stolfi sile lifestyle is the characteristic specific to ascidians among and Levine, 2011; Nishino et al., 2011; Ryan et al., 2016). By the tunicates. Other tunicate groups such as larvaceans and using the motor system, ascidians have a motile lifestyle at thaliaceans are planktonic throughout their life. The CNS of the larval stage. The shape of ascidian larvae is distinct from ascidian adults are small and short compared to their entire that of adults, and the distinctness has made it difficult to infer body size, and the dorsoventral axis of the CNS is not easy their relationships. to recognize from its outside morphology. This is in contrast The shape difference between larval and adult ascidians to the CNSs of other chordates; for example, the vertebrate is achieved by metamorphosis (Cloney, 1982). The ascidian CNS has a long spinal cord. A notochord is not found in adult larva possesses an adhesive organ named adhesive papilla at © The Sessile Organisms Society of Japan 2018 22 Sessile Organisms Vol. 35, No. 2, 2018 Fig. 1. Chordates, tunicates and ascidians. a: Phylogenetic position of tunicates in relation to the other chordate groups. b: Adults of the ascid- ian Ciona intestinalis Type A. c: A larva of Ciona intestinalis Type A. Green represents the position of the nervous systems. CNS, central ner- vous system. Fig. 2. The tunic of ascidians contains cellulose. a: A juvenile of C. intestinalis Type A. The animal is covered with the transparent tunic. This animal is approx. 1 week after fertilization, and the larval tail was lost by the metamorphic event. b: Cellulose staining of the larval tunic. The brown color represents the presence of cellulose. c: Schematic illustration of Ciona CesA protein. Left=the N-terminal of this protein. aa, amino acid. Cellulose and sessile lifestyle in ascidians 23 the anterior pole of the trunk (Fig. 1c). The adhesive papilla Ciona intestinalis, also possesses such a gene (Matthysse et secretes viscous substances, and the larva adheres to the sub- al., 2004). The genes are named CesA, with the abbreviated strate with the papilla. The papilla is a neuronal organ (Horie species names such as Ci-CesA. Genes encoding the protein et al., 2008), and adhesion is thought to be the stimulus that homologous to CesA were later detected in a non-ascidian starts the excitation of the neurons in the papilla. The excita- tunicate, the larvaceans Oikopleula dioica (Sagane et al., tion of the neurons could be transmitted toward the posterior 2010). The larvaceans do not settle, suggesting that they use part of the body through neurites (Takamura, 1998), and a set cellulose for a purpose other than settlement. Larvaceans have of metamorphic events is initiated. a special tunic structure called a ‘house,’ which is used for The outstanding metamorphic event of ascidians is the loss collecting food efficiently. Cellulose fibers are present in the of the tail. Most body parts of the adult ascidian are formed house (Kimura et al., 2001; Sagane et al., 2010). by the cells at the larval trunk supplemented by the ventrally The tunicate CesA proteins, which are seven-pass trans- located tail cells consisting of the endodermal strand and pri- membrane proteins, have a unique domain composition (Fig. mordial germ cells (Hirano and Nishida, 1997, 2000; Shirae- 2c). Their N-terminal region shows similarity to cellulose syn- Kurabayashi et al., 2006; Nakazawa et al., 2013; Kawai et thases of other organisms (Matthysse et al., 2004; Nakashima al., 2015). Other cells that form the larval tail are lost during et al., 2004; Sagane et al., 2010). Tunicate CesA proteins metamorphosis by tail regression and apoptosis (Chambon have the signatures of the GT-2 cellulose synthase family. et al., 2002, 2007). By this metamorphic alteration, ascidians The C-terminal region of tunicate CesA, by contrast, shows lose their apparent chordate features and motility to start ses- similarity to the cellulase domains of the GH-6 family. The sile life. coexistence of the domains whose deduced functions are com- For sessile organisms, protection of their body is essential pletely opposite is a unique characteristic of tunicate cellulose for defense against predators. Ascidians achieve this defense synthases. However, the GH-6 cellulase domains of tunicate by the tunic covering of their fragile body (Fig. 2a). The tu- CesA have mutations in the residues that are essential for the nic is the outmost layer of ascidians; it is not hard compared catalysis of the reaction of GH-6, suggesting that the domains to the shells of mollusks, but the tunic is so flexible that it is may not have the function of degrading cellulose (Matthysse not easily torn. The ascidian tunic contains cellulose (Fig. 2b; et al., 2004). Ranby, 1952), the organic macromolecule that is well known The finding of CesA genes in the genomes of tunicates sug- as the major component of cell walls of plant cells. Cellulose gests that tunicates can produce cellulose for themselves. This provides toughness to the ascidian tunic (Sasakura et al., hypothesis is supported by several lines of evidence. First, tu- 2005). The production of cellulose is not a specific feature of nicate CesA genes are expressed in the epidermis (Matthysse ascidians, and the ability to produce cellulose is shared among et al., 2004; Nakashima et al., 2004; Sagane et al., 2010). The tunicate groups (Hirose et al., 1999). However, among the epidermis is the outermost tissue that covers the entire body, chordates, the tunicates are the only group that synthesizes and it is in direct contact with the tunic; thus, the epidermis cellulose. This situation is not restricted to chordates; the is the strongest candidate for the source of cellulose. Sec- ability to produce cellulose is an exceptional characteristic of ond, CesA gene of Ciona savignyi (Cs-CesA) can rescue the tunicates among all animal groups. To understand the sessile cellulose-absent phenotype of the bacterium Agrobacterium lifestyle of ascidians, it is thus necessary to address the mech- tumefaciens (Matthysse et al., 2004).
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