The Evolving Proteome of a Complex Extracellular Matrix, the Oikopleura House

Abstract

Extracellular matrices regulate biological processes at the level of cells, tissues, and in some cases, entire multicellular organisms. The subphylum Urochordata exemplifies the latter case, where animals are partially or completely enclosed in “houses” or “tunics”. Despite this common strategy, we show that the house proteome of the appendicularian, Oikopleura, has very 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, with serial duplications up to 8 paralogs in one family. Expression pattern analyses revealed that individual oikosins are produced from specific fields of cells within the secretory epithelium, but in some cases, migrate up to at least 20 cell diameters in extracellular space to combine in defined house structures. Interestingly, peroxidasin and secretory phospholipase A2 domains, implicated in innate immune defence are secreted from the anlage associated with the food-concentrating filter, suggesting that this extra-organismal structure may play, in part, such a role in Oikopleura. We also show that sulfation of proteoglycans is required for the hydration and inflation of pre-house rudiments into functional houses. Though correct proportioning in the production of oikosins would seem important in repetitive assembly of the complex house structure, the genomic organization of oikosin loci appears incompatible with common enhancers or locus control regions exerting such a coordinate regulatory role. Thus, though all tunicates employ extracellular matrices based on a cellulose scaffold as a defining feature of the subphylum, they have evolved radically different protein compositions associated with this common underlying structural theme.

OikoBase: a genomics and developmental transcriptomics resource for the urochordate Oikopleura dioica

“…Despite this, animals continue feeding and replace their house regularly upon house degeneration and filter clogging, demonstrating continued house production even in the absence of apparent animal and cellular growth (Day2 dense to Day4 dense). The full expression profile of a structural component of the house, oikosin 19 (31) faithfully recapitulates all of these features (Supplementary Figure S1).

Figure 1.Complex developmental gene expression traffic in the compact O. dioica genome as visualized in the OikoBase genome browser.

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“…For example, a preliminary transcriptomics analysis shows that genes containing the most overrepresented domains (32) have highly clustered expression profiles, correlating well with the scaffolding of specific house substructures, a process that requires coordination of cell growth and positioning in addition to tuning of metabolic output within cell fields and between cell fields. The generation of multiple gene paralogs would allow for modulation of cell-specific functional output, as has previously been shown for paralogs of the house structural components, ‘oikosins’ (28,29,31). Numerous regulators of mitotic cell division have also been amplified in O. dioica (12), and our data indicate that expression of these paralogs is frequently anti-correlated, with novel variants expressed in non-mitotic tissues, such as endocycling cells and differentiating testes.…”

Phylogenetic analysis of phenotypic characters of Tunicata supports basal Appendicularia and monophyletic Ascidiacea

“…The character state in adults of the last common ancestor of Tunicata is not entirely obvious, because adult appendicularians feature a highly complicated secretion of the tunic that is based on the complexity and development of the filter‐feeding houses (Körner, ; Flood and Deibel, ). In addition, a duplication of cellulose synthase genes occurred in the stem lineage of appendicularians (Sagane et al., ; Hosp et al., ). Both facts show that the secretion of the tunic in adult Appendicularia is highly derived.…”

Mammoth grazers on the ocean's minuteness: a review of selective feeding using mucous meshes

“…Although gastropod mucus has been characterized-consisting of protein-polysaccharides, often with negatively charged acidic carbohydrates-the mucus of pteropod webs has not [110]. Benthic tunicate mucous meshes also contain acidic mucopolysaccharides and mucoproteins [77,111], but the molecular compositions of pelagic tunicate meshes appear to be quite distinct [112].…”