Ups and downs of intestinal function with prolonged fasting during aestivation in the burrowing frog, Cyclorana alboguttata

Abstract

SUMMARY Although green striped burrowing frogs (Cyclorana alboguttata)experience large reductions in the mass and absorptive surface area of the small intestine (SI) during aestivation, little is known about how this may affect the functional capacity of the SI. We examined changes in the function(l-proline uptake rate and capacity) and metabolism of the SI(in vitro oxygen consumption, Na+/K+-ATPase activity and abundance) of C. alboguttata following 6 months of aestivation. l-Proline uptake rate was significantly higher in aestivating frogs, but overall uptake capacity was lower than in active frogs. Total SI oxygen consumption rate (VO2) was also lower in aestivating frogs, despite no difference in mass-specific V̇O2. The proportion of intestinal V̇O2 associated with Na+/K+-ATPase activity and protein synthesis was equivalent between active and aestivating frogs, suggesting these processes were unaffected by aestivation. Indeed, the activity of Na+/K+-ATPase transporters in the SI of aestivating frogs was not different from that of active animals. Aestivating frogs maintained Na+/K+-ATPase activity, despite experiencing a reduction in the density of Na+/K+-ATPase transporters, by increasing the molecular activity of the remaining pumps to 2–3 times that of active frogs. These results show that functionality of the SI is maintained at the cellular level, potentially facilitating the reclamation of nutrients from the intestinal lumen while in aestivation. Despite this, the functional capacity of the SI in aestivating C. alboguttata is significantly reduced due to a reduction in tissue mass,helping frogs to conserve energy while in aestivation.

Mitochondria-Rich Cells: A Novel Type of Concealed Cell in the Small Intestine of Chinese Soft-Shelled Turtles (Pelodiscus Sinensis)

“…In our results, MRCs were characterized by the occurrence of an abundant quantity of mitochondria with high electron density in the cytoplasm relative to AECs and GCs. The intestinal epithelium of the chicken contains an abundance of mitochondria, i.e., 19% in MRCs and 10% in AEC [31]. In contrast, in our study, mitochondria were present at 35% in MRCs and at 20% in AECs.…”

“…MRCs are the sites for active ammonia elimination through the ion transport proteins, NKA and NKCC [35]. In the intestinal epithelium, the activity of NKA pumps helps to achieve a substantial portion of the total energy consumption by tissue [31]. Additionally, we observed two types of mitochondria in MRCs which were distinguished by their electron density and were adjoined to form intermitochondrial junctions (IJMs).…”

Epidermal epidemic: unravelling the pathogenesis of chytridiomycosis

“…This is consistent with the idea that the increase in I SC post-sloughing is the result of more functional transporters present in the new skin, although isotope binding studies (e.g. Cramp et al, 2009) would be needed to quantify this.…”

A unifying, eco‐physiological framework for animal dormancy

“…Many species cease all feeding at the onset of initiation (including one fish; Penttinen & Holopainen, 1992), and animals often dramatically decrease their digestive system volume (Cramp et al., 2009; Hahn & Denlinger, 2011; Hume et al., 2002; Martin et al., 2008; Naya et al., 2009). The gut microbiome of many animals is also modified as animals begin fasting during initiation (Bailey et al., 2010; Carey et al., 2013; Gossling et al., 1982; Liu et al., 2016; Secor & Carey, 2016; Sommer et al., 2016).…”

“…Many species cease all feeding at the onset of initiation (including one fish; Penttinen & Holopainen, 1992), and animals often dramatically decrease their digestive system volume (Cramp et al, 2009;Hahn & Denlinger, 2011;Hume et al, 2002;Martin et al, 2008;Naya et al, 2009).…”