Oxygen sensing in crustaceans: functions and mechanisms.

Animals that live in changing environments need to adjust their metabolism to maintain body functions, and sensing these changing conditions is essential for mediating the short- and long-term physiological and behavioral responses that make these adjustments. Previous research on nematodes and insects facing changing oxygen levels has shown that these animals rapidly respond using atypical soluble guanylyl cyclases (sGCs) as oxygen sensors connected to downstream cGMP pathways, and they respond more slowly using hypoxia-inducible transcription factors (HIFs) that are further modulated by oxygen-sensing prolyl hydroxylases (PHs). Crustaceans are known to respond in different ways to hypoxia, but the mechanisms responsible for sensing oxygen levels are more poorly understood than in nematodes and insects. Our paper reviews the functions of and mechanisms underlying oxygen sensing in crustaceans. Furthermore, using the oxygen sensing abilities of nematodes and insects as guides in analyzing available crustacean transcriptomes, we identified orthologues of atypical sGCs, HIFs, and PHs in crustaceans, including in their chemosensory organs and neurons. These molecules include atypical sGCs activated by hypoxia (Gyc-88E/GCY-31 and Gyc-89D/GCY-33) but not those activated by hyperoxia (GCY-35, GCY-36), as well as orthologues of HIF-α, HIF-ß, and PH. We offer possible directions for future research on oxygen sensing by crustaceans.

Emersion behavior of the semi-terrestrial crab Neohelice granulata during hypoxic conditions: Lactate as a trigger.

Climate changes affecting aquatic environments are increasing, and the resultant environmental challenges require animals to adopt alternative compensatory behavioral and physiological strategies. In particular, low levels of dissolved O2 are a regular problem for estuarine animals, leading to activation of a series of behavioral and physiological responses. This study on the semi-terrestrial crab Neohelice granulata examined patterns of emersion behavior under different levels of dissolved O2 availability and the role of lactate in this behavior. Emersion behavior was recorded for 4.5 h for crabs in water at four different levels of dissolved O2 (6, 3, 2, and 1 mg O2/L) and with free access to air. Oxygen consumption and hemolymphatic lactate levels were measured using the same experimental design. Emersion behavior was also recorded for 70 min in normoxic water after lactate or saline injections. Crabs increased their emersion behavior only in severe hypoxia (1 mg O2/L), and O2 consumption decreased under more severe hypoxic conditions. Despite the increase in emersion behavior, which leads to higher O2 availability, an increase in hemolymphatic lactate levels indicates that the animals still need to resort to anaerobic pathways to fulfill their metabolic demand. Furthermore, animals injected with lactate showed higher emersion behaviors than animals injected with a saline solution even in normoxia. These results suggest that the increase in hemolymphatic lactate can act directly or indirectly as a trigger for the increase in emersion behavior in the semi-terrestrial crab N. granulata.

Air exposure behavior of the semiterrestrial crab Neohelice granulata allows tolerance to severe hypoxia but not prevent oxidative damage due to hypoxia-reoxygenation cycle.

The air exposure behavior of the semi-terrestrial crab Neohelice granulata during severe hypoxia was studied. This study also verified whether this behavior mitigates possible oxidative damage, namely lipoperoxidation, caused by hypoxia and reoxygenation cycles. The lethal time for 50% of the crabs subjected to severe hypoxia (0.5 mgO2 · L(-1)) with free access to air was compared to that of crabs subjected to severe hypoxia without access to air. Crabs were placed in aquaria divided into three zones: water (when the animal was fully submersed), land (when the animal was completely emerged) and intermediate (when the animal was in contact with both environments) zones. Then the crabs were held in this condition for 270 min, and the time spent in each zone was recorded. Lipid peroxidation (LPO) damage to the walking leg muscles was determined for the following four experimental conditions: a--normoxic water with free access to air; b--hypoxic water without access to air; c--hypoxic water followed by normoxic water without air access; and d--hypoxic water with free access to air. When exposed to hypoxic water, N. granulata spent significantly more time on land, 135.3 ± 17.7 min, whereas control animals (exposed to normoxic water) spent more time submerged, 187.4 ± 20.2 min. By this behavior, N. granulata was able to maintain a 100% survival rate when exposed to severe hypoxia. However, N. granulata must still return to water after periods of air exposure (~ 14 min), causing a sequence of hypoxia/reoxygenation events. Despite increasing the survival rate, hypoxia with air access does not decrease the lipid peroxidation damage caused by the hypoxia and reoxygenation cycle experienced by these crabs.