Structure, function and cell dynamics during chaetogenesis of abdominal uncini in Sabellaria alveolata (Sabellariidae, Annelida)

Abstract

BackgroundDynamic apical microvilli of a single cell, called the chaetoblast, inside an ectodermal invagination form the template of annelid chaetae. Changes in the pattern of microvilli are frozen in time by release of chitin, such that the structure of the definitive chaeta reflects its formation. Cellular interactions during chaetogenesis also influence the structure of the chaeta. Analysing chaetogenesis allows for testing hypotheses on the homology of certain chaetal types. We used this approach to test whether the unusual uncini in Sabellaria alveolata are homologous to apparently similar uncini in other annelid taxa.ResultsOur study reveals unexpected details of sabellariid uncini, which mechanically reinforce the neuropodia enabling their use as paddles. The final structure of the chaeta is caused by pulses of microvilli formation and dynamic interaction between the chaetoblast and adjoining follicle cells. Cell dynamics during chaetogenesis of the uncini in Sabellaria alveolata exceeds by far that reported in previous studies on the formation of this type of chaetae.ConclusionDespite the superficial similarity of uncini in sabellariids and other annelids, differences in structure and details of formation do not support the homology of this type of chaetae. Chaetogenesis of sabellariid uncini involves unexpected microvilli and cell dynamics, and provides evidence that interactions between cells play a larger role in chaetogenesis than previously expected. In addition to their function as anchors, uncini in Sabellaridae stabilize the paddle-shaped notopodia, as each uncinus possesses a long, thin rod that extends deeply into the notopodium. The rods of all uncini in a single row form a bundle inside the notopodium that additionally serves as a muscle attachment site and thus have a similar function to the inner chaeta (acicula) of errant polychaetes (Aciculata).

Hairy and iridescent chaetae of the sea mouse Aphrodita (Annelida, Errantia)

“…In fact, it is not only the secretion of chaetal material but also the topology and dynamics of the follicle cells that influence the final shape and structure of the chaetae. This was particularly evident in the formation of abdominal uncini in Sabellaria alveolata (Linnaeus, 1767), described in Tilic and Bartolomaeus (2016). There, the follicle cells cover parts of the chaetoblast, directly interfering the microvillar template of the chaetoblast and resulting in the elongation of the chaetal rods.…”

“…The basalmost cell of this follicle is called a chaetoblast, and with dynamic apical microvilli, the chaetoblast forms the template of a developing chaeta (O'Clair & Cloney, 1974). The intricate machinery of chaetogenesis has been likened to a biological 3D printer (Warren, 2015), and it was characterized in great detail for various chaetal forms (Bartolomaeus, 1998; Hausen, 2005; Kolbasova et al., 2014; Tilic et al., 2014; Tilic et al., 2015; Tilic & Bartolomaeus, 2016).…”

The cellular 3D printer of a marine bristle worm—chaetogenesis in Platynereis dumerilii (Audouin & Milne Edwards, 1834) (Annelida)

“…Their enormous diversity primarily depends on the dynamics of the apical microvilli of the chaetoblast. Recent studies, however, showed that cellular interaction within and among chaetal follicles strongly influence the shape of the chaetae (Bartolomaeus 1998 ; Hausen 2005 ; Tilic et al 2014 , 2015 ; Tilic and Bartolomaeus 2016 ). These follicular interactions correlate with chaetal follicles that are arranged in a row running perpendicular or oblique to the body axis.…”

Desmosomal connectomics of all somatic muscles in an annelid larva

“…The position and density of desmosomes in muscle cells in the Platynereis larva suggest that these are the primary junctions mediating force transmission. Other types of junctions including various types of adherens-like junctions ( Tilic and Bartolomaeus, 2016 ) (primarily found in epidermal and chaetal follicle cells) were not considered here. Some adjacent muscle cells are also connected by an unclassified type of adhaerens-like junction (some examples are tagged with ‘junction type 3’ in the volume).…”