Evolutionary Adaptations of Parasitic Flatworms to Different Oxygen Tensions

Abstract

During the evolution of the Earth, the increase in the atmospheric concentration of oxygen gave rise to the development of organisms with aerobic metabolism, which utilized this molecule as the ultimate electron acceptor, whereas other organisms maintained an anaerobic metabolism. Platyhelminthes exhibit both aerobic and anaerobic metabolism depending on the availability of oxygen in their environment and/or due to differential oxygen tensions during certain stages of their life cycle. As these organisms do not have a circulatory system, gas exchange occurs by the passive diffusion through their body wall. Consequently, the flatworms developed several adaptations related to the oxygen gradient that is established between the aerobic tegument and the cellular parenchyma that is mostly anaerobic. Because of the aerobic metabolism, hydrogen peroxide (H₂O₂) is produced in abundance. Catalase usually scavenges H₂O₂ in mammals; however, this enzyme is absent in parasitic platyhelminths. Thus, the architecture of the antioxidant systems is different, depending primarily on the superoxide dismutase, glutathione peroxidase, and peroxiredoxin enzymes represented mainly in the tegument. Here, we discuss the adaptations that parasitic flatworms have developed to be able to transit from the different metabolic conditions to those they are exposed to during their life cycle.

Keywords: Cestoda; anaerobic metabolism; mitochondria; oxygen tension; platyhelminthes; tegument.

Figure 1

Life cycle of Taenia solium. Parasite stages and its migration through the interior of its intermediate host (e.g., pig, in green) and its definitive host (e.g., man, in purple), is illustrated.

Figure 2

Adult form of the cestodes is exposed to the intestinal oxygen concentration. The image shows a structural drawing of the adult tapeworm form of Echinococcus granulosus (left; size range 2–7 mm) and Taenia solium (right; size range 2–7 m), attacking the intestinal epithelium of their definitive host. Oxygen tension in the intestinal tissue decreases the further away parasites are from the intestinal capillaries, while the oxygen concentration in the intestinal lumen decreases as parasites move towards the colon, where the environment is practically anaerobic. Oxygen concentrations were obtained from references [33,34,35,36]. The size of the parasites was obtained from the Laboratory Identification of Parasites of Public Health Concern website (https://www.cdc.gov/dpdx/ (accessed on 17 February 2022)).

Figure 3

Tegument of the cestodes. Panel (a) represents a photograph of the tegument of Taenia crassiceps cysticercus obtained by transmission electron microscopy. Panel (b) is a schematic representation of the tegument of cestodes. Abbreviations: bl, basal lamina; er, endoplasmatic reticulum; gg, glycogen granules; M, muscle; MI, microtriches; N, nucleus; pm, parenchymal mitochondria (anaerobic mitochondria); tm, tegumental mitochondria (aerobic mitochondria); v, vesicles.

Figure 4

Aerobic and anaerobic energy metabolism in parasitic flatworms. Representation of the electron flow in aerobic metabolism: Panel (a), while Panel (b), represents the electron flow corresponding to anaerobic metabolism. Abbreviations: OMM, outer mitochondria membrane; IMM, inner mitochondria membrane; Ac-CoA, Acetyl coenzyme A; ASCT, acetate succinate-CoA transferase; cytc, cytochrome c; Fum, fumarate; FH, fumarate hydratase (fumarase); FRD, fumarate reductase; Glu-6-P, glucose 6-phosphate; Lac, lactate; LDH, lactate dehydrogenase; MDH, malate dehydrogenase; ME, mitochondrial malic enzyme; MetMal-CoA, methylmalonyl coenzyme A; Mlt, malate; PEP, phosphoenol pyruvate; PEPCK, phosphoenol pyruvate carboxykinase; PDH, pyruvate dehydrogenase complex; PK, pyruvate kinase; Pyr, pyruvate; OAA, oxaloacetate; RQ, rhodoquinone; Succ, succinate; Succ-CoA, succinyl-coenzime A; SDH, succinate dehydrogenase; TCA, tricarboxylic acid cycle; UQ, ubiquinone.

Figure 5

The antioxidant system of parasitic flatworms. Abbreviations: GSH reduced glutathione; GSSG, oxidized glutathione; H₂O₂, hydrogen peroxide; HO^●, hydroxyl radical; O₂, molecular oxygen; O₂^●− superoxide anion radical; Ph-GPx, glutathione phospholipid peroxidase; Prx, peroxiredoxin; SOD, superoxide dismutase; TGR, thioredoxin-glutathione reductase; Trx-(SH)₂, reduced thioredoxin; Trx-(S)₂, oxidized thioredoxin.