Adaptations for cryopelagic life in the antarctic notothenioid fish Pagothenia borchgrevinki

Summary The cryopelagic circumantarctic notothenioid fish Pagothenia borchgrevinki lives near the undersurface of the sea ice in McMurdo Sound, Antarctica. When compared to closely related benthic species (especially Trematomus bernacchii), Pagothenia exhibited substantial morphological differences in a variety of organ systems. The values of the fineness ratio and the indices of trunk shape and flatness suggested streamlining and drag reduction, adaptations to life in the water column. Pagothenia also lacked substrate contact adaptations in the pelvic and anal fins. Silvery reflective layers (strata argentea) beneath the skin and in the iris and choroid of the eye provided camouflage when Pagothenia were viewed against a background of platelet ice. The retina had many cones indicating the eye was adapted to both diurnal and nocturnal vision. During the austral spring Pagothenia fed exclusively on nektonic organisms near the ice-water interface. Dietary diversity was low; copepods and amphipods were the most frequently occurring and amphipods were the most frequently occurring taxa. In conclusion, Pagothenia appear specialized for life in the water column.     

Thermal sensitivity of scope for activity in Pagothenia borchgrevinki, a cryopelagic Antarctic nototheniid fish

The thermal sensitivity of scope for activity was studied in the Antarctic nototheniid fish Pagothenia borchgrevinki. The scope for activity of P. borchgrevinki at 0°C was 189 mg O₂ kg⁻¹ h⁻¹ (factorial scope 6.8) which is similar to that of temperate and tropical species at their environmental temperatures, providing no evidence for metabolic cold adaptation of maximum activity. The scope for activity increased to a maximum value of 266 mg O₂ kg⁻¹ h⁻¹ (factorial scope 8.3) at 3°C and then decreased from 3 to 6°C. The thermal sensitivity of critical swimming speed was also investigated and followed a similar pattern to aerobic scope for activity, suggesting oxygen limitation of aerobic performance. Oxygen consumption rates and ventilation frequencies were monitored for 24 h after the swimming challenge and the recovery of both parameters to resting levels was rapid and independent of temperature.     

Recovery from exhausting exercise in an Antarctic fish,Pagothenia borchgrevinki

Summary Pagothenia borchgrevinki, an Antarctic teleost fish was swum to exhaustion and changes in lactic acid levels and blood haematocrit were monitored during recovery. The fish did not perform well at high swimming speeds due to an inability of the white myotomal muscle to produce ATP by anaerobic glycolysis. Consequently, low levels of lactic acid were produced which were fairly rapidly broken down. Haematocrit values were low in non-exercised fish, and these increased by over 100% during exercise, falling back to control levels over many hours. This is probably related to the increased oxygen demand during exercise.     

Growth and reproduction of the Antarctic nototheniid fish Pagothenia borchgrevinki

Summary Growth and reproductive parameters were recorded from Pagothenia borchgrevinki captured from beneath the sea ice in McMurdo Sound during October and November 1987. Fish were aged on the basis of unvalidated check rings in otoliths. Fish were estimated to be 2–7 years old. There was good correlation of estimated ages with length-frequency modes for a number of year classes. Growth was linear, and did not approach an asymptote with increasing age. Most females were in the early stages of vitellogenesis, however, 2 fish showed evidence of imminent or recent spawning activity. Males were all in the early stages of spermatogenesis. Relative fecundity was low, and this was associated with large egg size. Ovarian development was group synchronous, and it appears that spawning mainly occurs during winter.     

X-cells in the gills of an Antarctic teleost, Pagothenia borchgrevinki

X-cell tumours have been described previously from teleost fish of the Northern Hemisphere, in which they occurred as lesions of the skin, pseudobranchs or gills. The present study describes X-cell tumours from the gills of an Antarctic teleost, Pagothenia borchgrevinki , thus extending the range to the Antarctic and also the Southern Hemisphere. Gills of affected fish were distinctly swollen and white in appearance, indicating that the gills were not functional as gas exchange organs. The affected gill tissue contained large numbers of X-cells, large spherical cells with a distinct extracellular coat and many densely staining membrane-bound granules. The possible origin of the cells is discussed.     

Haemoglobin of the antarctic fish Pagothenia bernacchii. Amino acid sequence, oxygen equilibria and crystal structure of its carbonmonoxy derivative.

The Antarctic fish Pagothenia bernacchii has one major haemoglobin, Hb1 (over 95% of the total blood content). Hb1 has a strong alkaline Bohr effect and at low pH exhibits the reduced ligand affinity and co-operativity that comprise the Root effect. We have determined the complete amino acid sequence of P. bernacchii Hb1 and also the structure of its carbonmonoxy derivative by X-ray crystallography, to a resolution of 2.5 A. The crystallographic R-factor of the refined structure is 18%. The three-dimensional structure of this fish haemoglobin is similar to that of human haemoglobin A, with a root-mean-square difference in main-chain atom positions of 1.4 A after superimposition of the two structures, despite only 48% homology of their amino acid sequences (including insertion of a single residue in the CD region of the fish alpha-chain). Large structural differences occur only at the N and C termini of both the alpha- and beta-chains. Neither these nor other smaller structural differences provide any obvious explanation of the Root effect of this or other fish haemoglobins.     

L-Glutamate dehydrogenase from the antarctic fish Chaenocephalus aceratus. Primary structure, function and thermodynamic characterisation: relationship with cold adaptation

In order to study the molecular mechanisms of enzyme cold adaptation, direct amino acid sequence, catalytic features, thermal stability and thermodynamics of the reaction and of heat inactivation of L-glutamate dehydrogenase (GDH) from the liver of the Antarctic fish Chaenocephalus aceratus (suborder Notothenioidei, family Channichthyidae) were investigated. The enzyme shows dual coenzyme specificity, is inhibited by GTP and the forward reaction is activated by ADP and ATP. The complete primary structure of C. aceratus GDH has been established; it is the first amino acid sequence of a fish GDH to be described. In comparison with homologous mesophilic enzymes, the amino acid substitutions suggest a less compact molecular structure with a reduced number of salt bridges. Functional characterisation indicates efficient compensation of Q(10), achieved by increased k(cat) and modulation of S(0.5), which produce a catalytic efficiency at low temperature very similar to that of bovine GDH at its physiological temperature. The structural and functional characteristics are indicative of a high extent of protein flexibility. This property seems to find correspondence in the heat inactivation of Antarctic and bovine enzymes, which are inactivated at very similar temperature, but with different thermodynamics.     

Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope

Fish larvae are the world's smallest vertebrates, and their high rates of mortality may be partially owing to a very limited aerobic scope. Unfortunately, however, no complete empirical dataset exists on the relationship between minimal and maximal metabolism (and thus aerobic scope) for any fish species throughout ontogeny, and thus such an association is hard to delineate. We measured standard and maximal metabolism in three marine fish species over their entire life history, and show that while aerobic scope depends greatly on body size and developmental trajectory, it is extremely small during the early life stages (factorial aerobic scope < or =1.5). Our findings strongly suggest that limited scope for aerobic activity early in life is likely to constrain physiological function and ultimately impact behaviour and possibly survival. Furthermore, our results have important implications for ecological models that incorporate metabolic scaling, and provide additional evidence against the existence of 'universal' scaling exponents.     

Gluconeogenic pathway does not display metabolic cold adaptation in liver of Antarctic notothenioid fish

Antarctic notothenioid fish display specializations related to cope with their chronically cold environment, such as high triacylglycerol (TAG) content in tissues. The metabolic fate of glycerol, a product of TAG mobilization, has not been studied in Antarctic fish. To assess the importance of glycerol as a substrate for gluconeogenesis and to determine whether this pathway is metabolically cold adapted (MCA), key hepatic enzyme activities were measured in Antarctic (Notothenia coriiceps, Gobionotothen gibberifrons, and Chionodraco rastrospinosus) and non-Antarctic (Dissostichus eleginoides, Patagonotothen ramsayi, and Eleginops maclovinus) notothenioid fish. Fructose 1,6-biphosphatase (FBP), phosphoenolpyruvate carboxykinase (PEPCK), and glycerol kinase (GK) activities were similar in both groups at common temperatures (1, 6, 11, or 21 °C). In particular, thermal sensitivity for the reactions catalyzed by FBP and PEPCK was analogous between Antarctic and non-Antarctic species, reflected by similar values for Arrhenius energy of activation (E _a) and Q₁₀. Additionally, hepatic glycerol, glucose, and glycogen contents together with plasma glycerol and glucose concentrations were similar for all of the species studied. Our results do not support the concept of MCA in hepatic gluconeogenesis and may indicate that the use of glycerol as a precursor for glucose synthesis by this pathway is of low physiological importance in Antarctic fish.     

The sarcoplasmic proteins of white muscle of an antarctic hemoglobin-free fish, Champsocephalus gunnari.

1. The protein composition of the sarcoplasm of Champsocephalus gunnari white muscle has been examined by ultracentrifugation and starch-gel electrophoresis. 2. The extracts have been fractionated by several methods in order to compare them more closely to similar extracts of other fish species and to isolate creatine kinase and the parvalbumins IV and V. 3. The creatine kinase does not appear to differ from other fish creatine kinases. Both parvalbumins are also very similar to other parvalbumins except that they are more easily oxidized than all the parvalbumins described so far.     

Absence of metabolic cold adaptation and compensatory acclimation in the Antarctic fly, Belgica antarctica

The respiratory metabolism in larvae of the Antarctic fly, Belgica antarctica Jacobs (Diptera: Chironomidae) was investigated at Palmer Station, Anvers Island (64°46′S, 64°03′W). Oxygen consumption was linearly related to temperature from 0 to 20°C, respectively, 49 and 338 nl/mg live wt/hr. Maintenance at 0 and 10°C for 8 days had no differential effect on the metabolic rate, suggesting that larvae lack the ability for compensatory acclimation. A comparison of standard metabolism for polar and temperate chironomids revealed no elevation of metabolic rate in polar forms. However, polar species exhibited lower activation energies than temperate forms indicating that the respiratory metabolism of polar chironomids is relatively temperature independent.     

Gene amplification and cold adaptation of pepsin in Antarctic fish. A possible strategy for food digestion at low temperature

Cold-adapted organisms have developed a number of adjustments at the molecular level to maintain metabolic functions at low temperatures. Among other features, they can produce enzymes characterized by a high turnover number or a high catalytic efficiency. The present work is aimed at investigating the process of food digestion at low temperature through the study of pepsins in Antarctic notothenioids. For such a purpose, we have cloned and sequenced three forms of pepsin A and a single form of gastricsin from the gastric mucosa of Trematomus bernacchii (rock cod). Phylogenetic analysis has suggested that the three pepsin A isotypes arose from two gene duplication events leading to the most ancestral pepsin A3 and to the most recent forms represented by pepsin A1 and pepsin A2. Molecular modeling has unraveled significant structural differences in these enzymes with respect to their mesophilic counterparts. Hydropathy and flexibility determined on the substrate-binding subsites of Antarctic and mesophilic pepsins have shown for pepsin A2 reduced hydropathy and increased flexibility at the level of the substrate cleft, features typical of cold-adapted enzymes. Northern blot analysis of RNA from rock cod gastric mucosa hybridized with molecular probes designed on specific regions of different pepsin forms has shown that rock cod pepsin genes are expressed at comparable levels. The present results suggest that the Antarctic rock cod adopted two different strategies to accomplish efficient protein digestion at low temperature. One mechanism is the gene duplication that increases enzyme production to compensate for the reduced kinetic efficiency, the other is the expression of a new enzyme provided with features typical of cold-adapted enzymes.