Aporocotyle simplex (Odhner, 1900)

Poddubnaya, Larisa G., Hemmingsen, Willy & MacKenzie, Ken, 2023, Digestive system of the marine blood fluke, Aporocotyle simplex (Odhner, 1900) (Digenea: Aporocotylidae) with consideration of the digenean digestive morphology, Zoologischer Anzeiger 305, pp. 11-22 : 19-20

4.4. Gastrodermal ultrastructural features of A. simplex

As shown in the present investigation, the lumen of four ramifications of the caecum in all studied specimens of A. simplex is filled with moderately dense amorphous finely dispersed material, in which dark inclusions and residual bodies are embedded. In A. simplex the luminal amplification of the syncytial gastrodermal lining is flexible lamellae, ranging in length from about 0.9 to 2.5 μm. A single cell type constitutes the digenean cellular or syncytial lamellated caecal epithelial lining (gastrodermis), the cytological nature of which changes with each phase of the digestive activity for both secretory and absorptive functions ( Davis et al., 1968; Robinson and Threadgold, 1975). As shown in our study, in the case of A. simplex , the secretory and absorptive functions in the gastrodermal syncytial epithelium may be observed along different regions of the caecum, performing both functions simultaneously. As noted by Robinson and Threadgold (1975), every gastrodermal cell (or gastrodermal syncytial region) shows an alternation in phases of its activity and the ability of the gastrodermis to perform some function. Robinson and Threadgold (1975) suggested that the various organelles of each gastrodermal region may reflect the physiological state of the particular region. Moreover, Davis et al. (1968) noted that secretory and nonsecretory digestive cycles exist in the cellular gastrodermis of the plagiorchiid, Heamatoechus medioplexus, and it is highly probable that both functions are performed simultaneously whenever food is present in the caecal lumen. The presence of a secretory cycle in the cellular gastrodermis of the plagiorchiid P. epiclitum was indicated by Mattison et al. (1992). In another plagiorchiid feeding on blood, Fellodistomum fellis , as in polyopisthocotylidean monogeneans, the digestive caeca consists of a layer of digestive cells overlain by a syncytial layer of connective tissue ( Halton, 1997). In contrast to polyopisthocotylideans, digestive cells possessing intracellular hemoglobin degradation (Konstanzov´a et al., 2015; Poddubnaya et al., 2015; Cable and El-Naggar, 2021) in F. fellis haemoglobin is not degraded within digestive cells, but is entrapped and digested within pockets formed by luminal lamellae, in which contents of zymogen-like granules are released with subsequent formation of residual haematin bodies. Such a type of digestion is called extracellular ( Halton, 1997). It should be emphasized that for the digeneans Bogitsh (1993) assumed the absence of intracellular digestion of exogenous food in the gastrodermis, but the presence of extracellular digestion in the caecal lumen, in so-called ‘superficial digestive vacuoles’ formed by the luminal lamellae. However, in other studies of blood flukes, the schistosomes demonstrated the acidic contents of their gastrodermis, suggesting that it is a site of hemoglobinolytic action and the enzymes secreted by the gastrodermis ( Bogitsh and Davenport, 1991). Distribution of acid phosphatase activity was associated with the luminal surface of the gastrodermis, gastrodermal lysosome-like structures such as the multivesiculate bodies, a variety of cytoplasmic vesicles and bodies in the schistosome gastrodermis ( Bogitsh and Shannon, 1971). Acid phosphatase was established as a marker for lysosomes and related organelles such as food vacuoles and may reflect the presence of a lysosome system in the digenean gastrodermis ( Ernst, 1975; Bogitsh and Ryckman, 1982). Moreover, the proteolytic pathway of hemoglobin digestion in the schistosome gastrodermis may indicate endopeptidase, as asparaginil, which has a pivotal role in haemoglobin digestion ( Dalton et al., 1995). In the gastrodermal cytoplasm of A. simplex there are extensive GER and Golgi complexes producing rounded vesicles (0.1–0.3 μm in diameter) containing an agglomeration of finely dispersed substance. In addition, the occurrence of multivesiculate bodies (0.4 μm in diameter), different kinds of residual bodies (2.0–2.6 μm in diameter), and large residual bodies (0.9–1.5 μm in diameter) may indicate the gastrodermal pathways of haemoglobin digestion in the studied marine aporocotylid species. The presence of protein synthesis in the gastrodermis is indicated by the observation that the enzymes enclosed within the Golgi vesicles are primary lysosomes ( Bogitsh and Davenport, 1991). As shown our investigation, haematin accumulates in the gastrodermal lumen of A. simplex . The fact that haematin occurs both intracellularly (within residual bodies) and within the gastrodermal lumen between lamellae may suggest the possibility that it is being moved across the membrane. As Morris (1968) postulated for schistosomes, and we assume it is true for the aporocotylid blood fluke, A. simplex , a combination of extra- and intracellular digestion occurs. Extracellular digestive enzymes produced by the esophagus initiate the digestion of hemoglobin, and the digestive process may then be completed after uptake by the gastrodermis, in which ‘an intermediate is phagocytosed and broken down to simple end products’ (see Morris, 1968, p. 482). Moreover, the presence of a number of regularly arranged tubular arrays in the gastrodermal cytoplasm of A. simplex may support a transport system of host proteins from the gastrodermal lumen to the intracellular reticular system of channels of gastrodermal cytoplasm.

Another aporocotylid species, the freshwater blood fluke S. inermis , has five, short, reduced intestinal outgrowths, the luminal surface of which lacks lamellae (McMichael et al., 1994a). In the brief description of the S. inermis intestine by McMichael et al. (1994a), the expanded cisternae of GER and Golgi complexes and electron-dense granules are restricted to some gastrodermal areas. However, these authors assumed that this is likely to facilitate food transport across the external tegument and might account for the reduction of the intestine and apical gastrodermal projections in the genus Sanguinicola . It is pertinent to note here that the previously published ultrastructural studies on the tegumental structure of the aporocotilid digeneans, A. simplex and S. inermis , have revealed no morphological evidence, which may reflect the physiological state for blood feeding through the tegument ( Poddubnaya et al., 2019; 2020b). Moreover, the distal cytoplasmic layer of these two aporocotylid digeneans is poor in organoids and vesicular inclusions. Further, using nucleotide pulse-chase, Lee (2023) noted that a large proportion of stem cells produce tegument precursors in schistosomula/juveniles. ‘Such continuous replenishment of stem cell-driven tegument cell production likely contributes to the schistosome’ s ability to evade host immunity’ ( Lee, 2023, p. 4). We may assume that the presence of short intestinal caeca in species of the genus Sanguinicola is a result of miniaturization of both body size and organs in the species of this genus. In any case, for freshwater species of the genus Sanguinicola , additional studies of the digestive system are required.