Formation of the hindgut cuticular lining during embryonic development of Porcellio scaber (Crustacea, Isopoda)

Abstract

The hindgut and foregut in terrestrial isopod crustaceans are ectodermal parts of the digestive system and are lined by cuticle, an apical extracellular matrix secreted by epithelial cells. Morphogenesis of the digestive system was reported in previous studies, but differentiation of the gut cuticle was not followed in detail. This study is focused on ultrastructural analyses of hindgut apical matrices and cuticle in selected intramarsupial developmental stages of the terrestrial isopod Porcellio scaber in comparison to adult animals to obtain data on the hindgut cuticular lining differentiation. Our results show that in late embryos of stages 16 and 18 the apical matrix in the hindgut consists of loose material overlaid by a thin intensely ruffled electron dense lamina facing the lumen. The ultrastructural resemblance to the embryonic epidermal matrices described in several arthropods suggests a common principle in chitinous matrix differentiation. The hindgut matrix in the prehatching embryo of stage 19 shows characteristics of the hindgut cuticle, specifically alignment to the apical epithelial surface and a prominent electron dense layer of epicuticle. In the preceding embryonic stage – stage 18 – an electron dense lamina, closely apposed to the apical cell membrane, is evident and is considered as the first epicuticle formation. In marsupial mancae the advanced features of the hindgut cuticle and epithelium are evident: a more prominent epicuticular layer, formation of cuticular spines and an extensive apical labyrinth. In comparison to the hindgut cuticle of adults, the hindgut cuticle of marsupial manca and in particular the electron dense epicuticular layer are much thinner and the difference between cuticle architecture in the anterior chamber and in the papillate region is not yet distinguishable. Differences from the hindgut cuticle in adults imply not fully developed structure and function of the hindgut cuticle in marsupial manca, possibly related also to different environments, as mancae develop in marsupial fluid. Bacteria, evenly distributed within the homogenous electron dense material in the hindgut lumen, were observed only in one specimen of early marsupial manca. The morphological features of gut cuticle renewal are evident in the late marsupial mancae, and are similar to those observed in the exoskeleton.

Ultrastructural differentiation of plasma membrane and cell junctions in the hindgut cells is synchronized with key developmental transitions in Porcellio scaber

“…The junctions between the apical plasma membrane and the cuticle were observed in P. scaber hindgut from the early-stage marsupial mancae onwards. This corresponds with the replacement of hindgut precuticular matrix in embryos with the first hindgut cuticle in earlystage marsupial mancae (Mrak et al, 2015). In postmarsupial mancae and adult animals (Bogataj et al, 2018) these junctions ultrastructurally resemble connections with the cuticle in epidermal tendon cells, which serve as attachments of muscles to exoskeleton (Žnidaršič et al, 2012).…”

Comparative ultrastructure of cells and cuticle in the anterior chamber and papillate region of Porcellio scaber (Crustacea, Isopoda) hindgut

“…The hindgut cuticle is thin and consists of two distinct layers, the electron dense epicuticle facing the lumen and the electron lucent procuticle beneath. Posteriorly directed cuticular spines are present at the surface of epicuticle (Vernon et al 1974, Palackal et al 1984, Storch and Štrus 1989, Mrak et al 2015). The main ultrastructural characteristics of hindgut epithelial cells are the extensively infolded apical and basal plasma membranes, numerous mitochondria associated with membrane infoldings, abundant apico-basally oriented microtubules, and extensive septate junctions (Vernon et al 1974, Coruzzi et al 1982, Palackal et al 1984, Storch and Štrus 1989).…”

Roles of LmCDA1 and LmCDA2 in cuticle formation in the foregut and hindgut of Locusta migratoria

“…Some data are available from a study on the hindgut of the crustacean isopod Porcellio scaber . Here, during cuticle differentiation from the prehatching embryonic to the marsupial manca stage, the chitin matrix of the procuticle remains unorganized (Mrak et al ., 2015). Because of the scarce data available, discussion of general and specific features of gut development in insects is not possible.…”