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M444p263.Pdf Vol. 444: 263–274, 2012 MARINE ECOLOGY PROGRESS SERIES Published January 10 doi: 10.3354/meps09379 Mar Ecol Prog Ser Enhancing thermal tolerance by eliminating the pejus range: a comparative study with three decapod crustaceans Jennifer A. Jost1,2, Stephanie M. Podolski1, Markus Frederich1,* 1Department of Marine Sciences, University of New England, Biddeford, Maine 04005, USA 2Present address: Biology Department, Bradley University, Peoria, Illinois 61625, USA ABSTRACT: Marine invertebrates in the intertidal and subtidal zones are often exposed to highly variable environmental conditions, especially rapid changes in temperature. The ability to survive at different temperatures has previously been described using an extended version of Shelford’s law of tolerance, with optimum, pejus (Latin: ‘turning worse’), and pessimum ranges, and the respective thresholds, critical (Tc) and pejus (Tp) temperatures, that mark the transition from one range into the next. The width of the pejus range, in which the scope for activity gradually declines, varies among species. We tested the hypothesis that the width of the pejus range is cor- related to the temperature stability of the species’ respective habitats. We used locomotor activity, heart rate, lactate accumulation, heat shock protein 70 (HSP70) levels, and the activation of AMP- activated protein kinase (AMPK) to identify Tc and Tp in 3 decapod crustaceans: green crab Carci- nus maenas, rock crab Cancer irroratus, and lobster Homarus americanus. We found species- specific patterns of temperature-induced changes in all parameters, especially in HSP70 protein and AMPK activity. The width of the pejus range (between Tp and Tc) was 8 to 12°C for rock crabs and 12 to 16°C for lobsters. Most importantly, green crab, the most temperature-tolerant of our 3 species and which lives in a highly variable habitat, switched directly from optimum to pessimum range, meaning that the pejus range was eliminated completely. Additionally, even lethal temper- atures did not activate AMPK in green crabs, pointing to a different cellular tolerance strategy than in rock crabs and lobsters. This modified tolerance pattern might represent a broader strategy to enhance physiological tolerance in a highly variable habitat. KEY WORDS: AMP-activated protein kinase · AMPK · Heat shock protein 70 · HSP70 · Temperature stress · Critical temperatures Resale or republication not permitted without written consent of the publisher INTRODUCTION to the low ATP yield of anaerobiosis that exacerbates the mismatch of energy supply and demand at Marine invertebrates are often exposed to varying extreme temperatures. This concept is supported by temperatures and have evolved strategies to tolerate work on several marine invertebrate and fish spe- these changes. During severe heat stress, the failure cies (for review see Pörtner 2002, 2010). The con- of ventilatory or circulatory function results in a tran- cept of Tc is consistent with Shelford’s law of toler- sition to anaerobic metabolism even if sufficient oxy- ance (Shelford 1931), which states that an animal gen for aerobic metabolism is present in the environ- or plant performs well in an optimum range for any ment. The threshold at which this transition occurs is given environmental parameter, such as tempera- defined as the critical temperature (Tc) (Zielinski & ture. Outside the optimum range, performance grad- Pörtner 1996). Survival beyond Tc is time-limited due ually declines, and is very poor in the pessimum *Corresponding author. Email: [email protected] © Inter-Research 2012 · www.int-res.com 264 Mar Ecol Prog Ser 444: 263–274, 2012 ranges at both extremes. Tc characterizes the transi- physiology level, and the cellular-molecular level. We tion into the pessimum range. However, in its natural used a broad set of whole-animal level and cellular environment an animal is frequently exposed to sub- parameters to identify Tp and Tc. optimal conditions, often well before Tc is attained. Consequently, Frederich & Pörtner (2000) added ‘pe- jus temperature’ (Tp) and ‘pejus range’ (from the MATERIALS AND METHODS Latin for ‘turning worse’) to this concept. In the pejus range, which is between the optimum and pessimum Animals ranges, animals can still survive, but with a reduced scope for aerobic activity. Subsequent studies have Adult rock crabs Cancer irroratus (Say, 1817) with identified Tp and pejus ranges in various species an average carapace width of 9.3 ± 1.3 cm (mean ± of marine invertebrates and fish (reviewed by Pört- SD) were acquired as bycatch in lobster traps by a lo- ner 2010). Tp and Tc differ by several degrees, thus cal lobster fisherman in Saco, Maine. Adult intermolt in dicating a well-defined and broad pejus range. green crabs Carcinus maenas (Linnaeus, 1758) with However, the width of the pejus range appears to an average carapace width of 4.5 ± 0.7 cm were col- vary among species, and the outstanding question of lected by hand in the intertidal of Biddeford Pool, whether this is associated with habitat stability needs Maine. Adult hard shell lobsters Homarus ameri- to be addressed. canus (Milne Edwards, 1837) with an average cara- In a previous study on the rock crab Cancer irrora- pace length of 8.9 ± 0.2 cm were trapped by a local tus, we showed that Tp can be identified on the cellu- lobster fisherman off Winter Harbor, Maine. All ani- lar level by the activity of AMP-activated protein mals were collected during June and September of kinase (AMPK; Frederich et al. 2009). AMPK is a 2008 and 2009 and kept in a flowthrough seawater well-characterized ‘master switch’ for cellular energy system in the Marine Science Center at the Uni - metabolism in mammals (Winder & Hardie 1999). versity of New England (UNE), with ambient sea - AMPK is thought to constantly monitor the energy water temperatures of 12 to 15°C and salinity 30, status of a cell and to regulate the anabolic and cata- and fed squid, mussels, and fish ad libitum. Animals bolic processes to ensure a constant ATP concentra- were used for experimentation after at least 1 wk of tion. The activation of AMPK prevents ATP depletion acclimation. and promotes replenishing of the ATP pool by inhibiting ATP-consuming pathways such as the syn- thesis of glycogen, fatty acids, proteins, and choles- Sequencing terol, and in parallel, accelerating ATP-producing pathways such as glucose uptake, glycolysis, and To design degenerate primers, we searched Gen- fatty acid β-oxidation. AMPK is highly conserved Bank for AMPK protein sequences from various during evolution, and similar functions have been invertebrate and vertebrate species. Obtained sequ - identified in mammals, birds, Caenorhabditis ele- ences were aligned using the MultAlin tool (http: // gans, the fruit fly, yeast, and other species (for review bioinfo.genotoul.fr/multalin/multalin.html). De gen - see Karagounis & Hawley 2009 or Hardie 2011). er ate forward and reverse primers for PCR were For the present study, we investigated how the designed based on highly conserved areas in the width of the pejus range varies in 3 decapod crus- aligned sequences. tacean species with different habitat-usage patterns. For all 3 species, total RNA from the hepatopan- We tested the hypothesis that the highly temperature- creas was purified using the Total RNA Isolation Sys- tolerant intertidal green crab Carcinus maenas has a tem (Promega) and reverse-transcribed (Super-Script broader pejus range than the rock crab Cancer irrora- First Strand Synthesis System, Invitrogen). We ampli- tus, which lives largely in the subtidal and moves only fied cDNA with the respective primer pairs via PCR occasionally into the intertidal zone. The American with an annealing temperature of 45°C. Resulting lobster Homarus americanus, as an entirely subtidal bands were extracted and DNA purified using the animal, was hypothesized to have the narrowest pejus MinElute Gel Extraction Kit (Qiagen). DNA was range. Subtidal habitats typically exhibit fewer and sequenced at the Mount Desert Island Biological slower water-temperature fluctuations than intertidal Laboratory sequencing core facility (MDIBL, Salis- habitats. We exposed the animals to a fast and pro- bury Cove, ME) on an ABI 3100 sequencer. The gressive temperature challenge and measured para- obtained DNA sequences were converted to a pre- meters at the behavioral level, the whole-animal dicted amino acid sequence using the NCBI open Jost et al.: Temperature tolerance in crustaceans 265 reading frame finder (www.ncbi.nlm.nih.gov/gorf/ above the heart, as described in detail by Depledge gorf. html), and a BLAST search confirmed the cDNA (1984) and Frederich & Pörtner (2000), and con- as AMPK (as per the methods in Towle et al. 2001). nected to a digital recording device (PowerLab). Average heart rate was determined for each species every 2°C during heating by counting peaks manu- Temperature incubations ally over a 1 min period. For the temperature range in which the data follow a linear regression, the Q10 was Animals (5 per species and time point) were calculated using the equation from the respective placed overnight in a darkened 100 l tank at 12°C. regression. The following day, animals were exposed to a fast, progressive temperature increase (6°C h−1) and sac- rificed at 12, 14, 16, 18, 20, 22, 24, 26, 28, 30, 32, or Lactate 34°C (not all temperatures were used for each spe- cies). Animals were sacrificed at the respective Lactate concentration, indicating the onset of temperature with a cut through the cerebral gan- anaerobiosis, was measured in the harvested heart glion and the heart was removed and flash-frozen tissue for each species using a photometric enzyme with Wollenberger tongs pre-cooled in liquid nitro- assay that quantifies the accumulation of NADH after gen. The flash-frozen samples were stored at converting lactate and NAD into pyruvate and −80°C. We focused on the heart tissue because a NADH (Bergmeyer 1985) and normalized to protein functioning circulatory system is crucial for main- concentration (Bradford 1976).
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