The lungs of Polypterus senegalus and Erpetoichthys calabaricus: Insights into the structure and functional distribution of the pulmonary epithelial cells

Abstract

The present article is a comparative, structural study of the lung of Polypterus senegalus and Erpetoichthys calabaricus, two species representative of the two genera that constitute the Polypteriformes. The lung of the two species is an asymmetric, bi-lobed organ that arises from a slit-like opening in the ventral side of the pharynx. The wall is organized into layers, being thicker in P. senegalus. The inner epithelium contains ciliated and non-ciliated bands. The latter constitute the respiratory surface and are wider in E. calabaricus. The air-blood barrier is thin and uniform in P. senegalus and thicker and irregular in E. calabaricus. In the two species, the ciliated areas contain ciliated cells, mucous cells and cells with lamellar bodies. Additionally, P. senegalus contains polymorphous granular cells (PGCs) and neuroendocrine cells (NECs) while E. calabaricus lacks PGCs but shows granular leukocytes and a different type of NEC. Interestingly, ciliated cells and secretory cells show a dual morphology in E. calabaricus indicating the presence of cellular subtypes and suggesting more complex secretory activity. Also in E. calabaricus, cilia show a novel doublet-membrane interaction that may control the displacement of the microtubule doublets. The subepithelium is a connective layer that appears thicker in P. senegalus and contains, in the two species, fibroblasts and granulocytes. The outer layer contains bundles of richly innervated striated muscle. This layer is likely involved in the control of lung motion. In the two species, smooth muscle cells constitute a limiting layer between the subepithelium and the striated muscle compartment. The role of this layer is unclear.

The gas bladder of Pantodon buchholzi: Structure and relationships with the vertebrae

“…However, this feature is not unique to Pantodon . It has also been observed in the lungs of Caudata (Goniakowska‐Witalinska, 1980), and in the lung of the polypterid Erpetoichthys calabaricus (Icardo et al, 2017).…”

“…In non‐mammalian vertebrates, ciliary rootlets were considered to be a distinct characteristic of the ciliated cells of the amphibian lung (Goniakowska‐Witalinska, 1995). However, they appear to be a general feature since they are also present in the polypterid lung (Icardo, Colvee, Kuciel, Lauriano, & Zaccone, 2017), and in the gas bladder of the spotted gar (Icardo et al, 2015). The presence of lamellar bodies in ciliated cells indicates a secretory role.…”

“…It is possible that Pantodon is an example in which a role in the decrease of wall surface tension is not necessary due to the anatomical characteristics of the respiratory organ. Rather, the surfactant may protect the luminal epithelium from tissue oxidative damage, maintain humidity and avoid wall adherence during bladder motion (Hughes & Weibel, 1978; Icardo et al, 2017). The possibility that the surfactant may spread over the dorsolateral wall of the bladder should also be considered.…”

Lung evolution in vertebrates and the water-to-land transition

“…Curiously, some living vertebrates display an unpaired organ (Cupello et al, 2015; Cupello et al, 2017a; Cupello et al, 2017b; Cupello, Clément and Brito, 2019; Lambertz and Perry, 2015; Lambertz et al, 2015), leaving the ancestral condition equivocal. The sister group to all other extant actinopterygians, the obligate air-breathing polypterids (Icardo et al, 2017), breath air using lungs, which have previously been described as a paired organ (Icardo et al, 2017; Geoffrey Saint Hilaire, 1802; Graham, 1997). However, in adult specimens of Polypterus senegalus the glottis only opens to the right sac and the left sac is connected to the right sac by a separate opening (Graham, 1997), raising old questions about its true paired condition.…”

The vestigial lung of the coelacanth and its implications for understanding pulmonary diversity among vertebrates: new perspectives and open questions

“…One of the most interesting aspects of the coelacanth is that it apparently exhibits an unpaired structure of putative homology with lungs [6][7][8]. In the Polypteriformes (bichir and reed fish), the lungs are paired [5,9,10], as are those of the lungfishes (Dipnoi) [11], except the Australian lungfish, Neoceratodus forsteri (Krefft, 1870) [12], in which only the right lung persists [11,13]. The Anlage of a left lung, however, is formed during early ontogeny also in this species, but rapidly degenerates during progressed development [13].…”