Thompson Group - Engineering of a complex extracellular structure, the Oikopleura house

Cellulose synthase (CesA) gene products are present in filter-feeding structures of all tunicates and the single CesA gene in the ascidian Ciona, also regulates metamorphosis. There are two CesA genes in the sister class, larvacean, O. dioica. Od-CesA1 produces long cellulose fibrils along the larval tail whereas Od-CesA2 is responsible for the cellulose scaffold of the post-metamorphic filter-feeding house. Phylogenetic analyses indicate that a single lateral gene transfer event from a prokaryote at the base of the lineage conferred biosynthetic capacity in all tunicates (Fig. 1). The horizontal transfer of a prokaryotic gene giving rise to the extant tunicate CesAs is more than a mere curiosity. It has been speculated that the ability to secrete a protective covering could have impacted life history strategies by prohibiting larval feeding and increasing evolutionary pressure on speed of development. Thus, relative to other chordates, the notable acceleration of tunicate development, greatly accentuated in the fully planktonic larvaceans, might have been triggered by the ability to secrete a tunic. In a larger sense, tunicates, which are uniformly filter-feeders, have combined cellulose synthesis with cellular mechanisms enabling the elaboration of complex extracellular structures, some of which are invariably associated with the filter-feeding mechanism. The sister vertebrates, lacking cellulose synthetic capability, exhibit a variety of more active feeding mechanisms, including filter-feeding, and have undergone elaboration of skeletal, sensory and nervous systems compared with tunicates and the chordate ancestor. Arguably, the lateral gene transfer event has had a profound influence on the tunicate lineage, which has undergone secondary morphological simplification and is evolving at faster evolutionary rates than their vertebrate cousins.

Tunicate CesA origins
Fig. 1 Origin of cellulose synthase (CesA) genes in the tunicate lineage. CesA genes containing glycosyltransferase 2 (GT-2) domains are found in bacteria, plants, amoebae and tunicates. Many bacterial cellulose synthase and endoglucanase genes are contained in single operons. Our data support horizontal transfer of a prokaryotic CesA-like gene to the common ancestor of tunicates. The gene(s) responsible for cellulose production in thaliaceans have not yet been isolated. Large view

Despite this common “tunicate” strategy, the proteome of the Oikopleura house has little in common with the proteome of the sister class, ascidian, Ciona. Of 80 identified house proteins (oikosins), ~half lack domain modules or similarity to known proteins, suggesting de novo appearance in appendicularians. Gene duplication has been important in generating almost 1/3 of the current oikosin complement. Correct proportioning in the production of oikosins would seem important in repetitive assembly of the complex house structure, but the genomic organization of oikosin loci appears incompatible with common enhancers or locus control regions exerting coordinate regulation.

We also examine cellular mechanisms for templating extracellular cellulose microfibrils in animal cells compared to current models in phylogenetically distant plants. Through targeted disruption of cytoskeletal elements, secretory pathways, and plasma membrane organization we propose a working model (Fig. 2) that shows some convergence but also significant differences with plant models. A specialized cortical F-actin array is implicated in templating cellulose microfibril orientation and GPI-anchored proteins in mobile lipid rafts may act as scaffolding proteins in microfibril elongation. Microtubules appear to be involved in delivery and maintenance of cellulose synthase complexes to specific sites on the cell membrane rather than orienting movement of these complexes through the membrane. At present it would appear that while employing the common cellulose building block, urochordates have been innovative in incorporating various structural domains into original extracellular proteins for specific architectural solutions in the three main lineages.

cloned cDNA

Fig. 2. Model for ordered incorporation of cellulose microfibrils into the inlet filter of the Oikopleura dioica house. Directions of weft and warp threads of the mesh are indicated by green double-headed arrows. The apical region of one of three central giant Eisen cells is shown abutting a second giant cell and surrounding cells of the Eisen field. The apical cortical array of F-actin in giant cells guides the orientation of weft-thread elongation, either via transmembrane scaffolding proteins or complexes that link extracellular scaffolding proteins to membrane proteins organized by the underlying F-actin network. Microtubules in surrounding cells sort the CesA units to correct sites on the plasma membrane where microfibril synthesis originates. Lipid rafts in the apical giant cell plasma membrane surface are involved in warp-thread elongation across adjacent cells. Golgi-sorted proteins provide the links between transverse F-actin fibres, lipid rafts, and cellulose microfibril orientation. Larger view

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