Tissue-dependent variations of hydrogen sulfide homeostasis in anoxic freshwater turtles

Abstract

Hydrogen sulfide (H 2 S) controls numerous physiological responses. To understand its proposed role in metabolic suppression, we measured free H 2 S and bound sulfane sulfur (BSS) in tissues of the freshwater turtle Trachemys scripta elegans, a species undergoing strong metabolic suppression when cold and anoxic. In warm normoxic turtles, free H 2 S was higher in red blood cells (RBCs) and kidney (∼9-10 µmol l −1 ) than in brain, liver and lung (∼1-2 µmol l −1 ). These values overall aligned with the tissue H 2 S-generating enzymatic activity. BSS levels were similar in all tissues (∼0.5 µmol l −1 ) but ∼100-fold higher in RBCs, which have a high thiol content, suggesting that RBCs function as a circulating H 2 S reservoir. Cold acclimation caused significant changes in free and bound H 2 S in liver, brain and RBCs, but anoxia had no further effect, except in the brain. These results show tissue-dependent sulfide signaling with a potential role in brain metabolic suppression during anoxia in turtles.

Exploring pathways of NO and H2S signaling in metabolic depression: The case of anoxic turtles

“…4). In addition, the minor fraction of Hb containing a ferric heme (~1%) can also act as a reversible carrier of H2S in the blood Fago, 2020, 2018), consistent with high measured levels of free H2S (~20 µM) in turtle RBCs (Jensen et al, 2019). Although these values appear exceedingly high compared to those found in other vertebrates, it is important to keep in mind that these levels correspond to max 0.5% of total Hb thiol persulfidation and to max 10% of ferric heme bound to H2S, which are not unrealistic considering estimates of 10-25% persulfidation in other less abundant proteins (Mustafa et al, 2009).…”

“…A consequence of the high thiol content of turtle RBC is the high capacity of carrying high levels of sulfide (as persulfide and polysufide) bound to the Hb molecule, as found in normoxic and anoxic Trachemys turtles (Jensen et al, 2019) (Fig. 4).…”

Hydrogen sulfide exposure reduces thermal set point in zebrafish

“…By contrast, ectotherms like fish behaviourally defend their thermal preference, enabling direct assessment of body temperature regulation. Whereas in most terrestrial animals exogenous H 2 S is applied to study the gasotransmitter's endogenous functions [8,9], exogenous H 2 S is ecologically relevant in aquatic habitats [11][12][13][14]. We exploit this physiology as a direct test of the hypothesis that H 2 S drives changes in thermal preferences, which is significant for the ecology and behaviour of this major taxon.…”

Cytoskeletal Arrest: An Anoxia Tolerance Mechanism

“…This suggests a role for H 2 S production in anoxic calcium signalling in turtle brain. Coupled with the above finding of increased bound H 2 S in cold-acclimated turtle brain [ 229 ], H 2 S is implicated in the regulation of metabolic depression in turtles. Whether H 2 S-induced calcium increase disrupts the cytoskeleton, or whether H 2 S inhibits RhoA, remains to be tested in turtles.…”

“…Strangely, the combination of cold and anoxic acclimation results in free and bound H 2 S levels that do not differ significantly from normoxia. In turtle erythrocytes cold increases both free and bound H 2 S, but there is no further increase with cold anoxia [ 229 ]. This suggests a possible role of circulating H 2 S in cold-tolerance, but implications for anoxia are unclear.…”