Metabolic depression is delayed and mitochondrial impairment averted during prolonged anoxia in the ghost shrimp, Lepidophthalmus louisianensis (Schmitt, 1935)

Abstract

Lepidophthalmus louisianensis burrows deeply into oxygen-limited estuarine sediments and is subjected to extended anoxia at low tides. Large specimens (>2 g) have a lethal time for 50% mortality (LT 50 ) of 64 h under anoxia at 25º C. Small specimens (<1 g) have a significantly higher LT 50 of 113 h, which is the longest ever reported for a crustacean. Whole body lactate levels rise dramatically under anoxia and exceed 120 µmol g.f.w. −1 by 72 h. ATP, ADP, and AMP do not change during 48 h of anoxia, but arginine phosphate declines by over 50%. Thus arginine phosphate may help stabilize the ATP pool. Surprisingly, when compared to the aerobic resting rate, ATP production under anoxia is unchanged during the first 12 h, and drops to only about 50% between 12 and 48 h. Finally, after 48 h of anoxia, a major metabolic depression to less than 5% occurs. Downregulation of metabolism is delayed in L. louisianensis compared to many invertebrates that exhibit facultative anaerobiosis. Bioenergetic constraints as a result of eventual metabolic depression led to ionic disturbances like calcium overload and compromised membrane potential of mitochondria. Because these phenomena trigger apoptosis in mammalian species, we evaluated the susceptibility of ghost shrimp mitochondria to opening of the mitochondrial permeability transition pore (MPTP) and associated damage. Energized mitochondria isolated from hepatopancreas possess a pronounced capacity for calcium uptake. Exogenous calcium does not stimulate opening of the MPTP, which potentially could reduce cell death during prolonged anoxia.

Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish

“…It would be good to understand why the transition pore in A. franciscana is resistant to opening and what structural differences might exist for its ATP synthase. A similar lack of calcium-induced opening has been observed for mitochondria of the ghost shrimp, Lepidophthalmus louisianensis (Holman and Hand, 2009). While no direct evidence exists concerning opening of the transition pore in embryos of A. limnaeus, they are highly resistant to anoxia-induced apoptosis (Meller and Podrabsky, 2013), and thus may share similar resistance to mitochondrial-induced apoptosis.…”

Developmental changes in hypoxic exposure and responses to anoxia in Drosophila melanogaster

“…In turtles, plasma lactate can accumulate to 150-200 mmol l −1 , but this requires 3-5 months of anoxia at 3°C (Jackson, 1997). Ghost shrimp, which live in marine sediments and are highly tolerant of anoxia, accumulate 120 mmol lactate kg −1 in about 50 h, a lactate accumulation rate 1/25 that of anoxic Drosophila larvae (Holman and Hand, 2009). The only comparable rate of lactate formation during anoxia ever reported for animals was for Culex pipiens mosquito larvae, which accumulated lactate at a rate of about 55 mmol kg −1 h −1 (measured over a period of 1.5 h) (Redecker and Zebe, 1988), a value quite similar to that shown here for Drosophila larvae.…”

“…Vertebrates with good capacities to survive and down-regulate metabolism in anoxia such as turtles and goldfish can reduce their metabolic rates in anoxia to 10-30% of resting aerobic rates (Herbert and Jackson, 1985;van Ginneken and van den Thillart, 2009). Similarly, the marine priapulid worms Sipunculus nudus and Halicryptus spinulosus, the ghost shrimp Lepidophthalmus louisianensis and the bivalves Astarte borealis and Arctica islandica lower their metabolic rates to 20-60% of aerobic rates after 1 day or less of anoxia (Hardewig et al, 1991;Holman and Hand, 2009;Oeschger, 1990). Marine mollusks such as Mytilus edulis and Acanthocardia tuberculata reduce their metabolic rates even lower, to 5-6% of aerobic rates during multiple hours of anoxia (Theede, 1984;Theede et al, 1969).…”

Lactate accumulation in the intertidal hermit crab, <i>Pagurus samuelis</i>, in response to burial-induced hypoxia

“…Anaerobiosis was shown to occur in crustaceans in conditions, such as exercise (Briffa & Elwood, 2001;Full & Herreid, 1984;Henry et al, 1994;McDonald et al, 1979;Smatresk et al, 1979), aerial exposure (Ridgway et al, 2006), and hypoxia (Butler et al, 1978;Hervant et al, 1995;Holman & Hand, 2009). The crustacean physiological response to functional and environmental hypoxia is similar to that in vertebrates.…”