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Investigations on the sources utilized for the energy supply fuelling the jump of springtails

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Abstract

In order to analyse the energy providing metabolites fuelling the jump of springtails, jumping experiments have been performed with two groups of springtails, Arthropleona and Symphypleona, which differ in their morphology and behaviour. During rest, the level of adenine nucleotides, especially ATP, in the Arthropleona species, Tomocerus flavescens and Orchesella cincta, is higher than that in the Symphypleona species, Allacma fusca and Dicyrtoma fusca. After a series of jumps a significant decrease of ATP appears in all investigated species while ADP and AMP increase. Phosphoarginine was high during rest in all investigated animals, and depleted after a series of jumps while the concentration of arginine increased simultaneously. Changes in both metabolite types are most pronounced in the Arthropleona. The amount of l-lactate, measured in Orchesella cincta, showed no significant changes. The results suggest that the muscles performing the jump of springtails belong to the type of muscles that are specialized to anaerobic “burst” activity. However, in the Symphypleona species, which are characterized by a more effective oxygen supply, the acquisition of energy may also occur through aerobic metabolism.

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... S pringtails (Arthropoda:Collembola) are the most widespread, abundant and diverse group of non-insect hexapods on the planet, which are known for their major role in soil ecology, and unique adaptions to catapult themselves into the air (1). Collembolans' jumping performance has been extensively studied in terms of locomotion (2)(3)(4), morphology (4)(5)(6), behavior (7)(8)(9), energetics (10), and computational modeling (11). It has inspired the design of mechanical jumpers (12,13) and robots (14). ...
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Article
1. Concentration changes of phosphagen (arginine phosphate) and adenine nucleotides (ATP, ADP, AMP) and Pi, some glycolytic and Krebs cycle intermediates, d-lactate, and carbohydrate substrates were measured in the prosomas and legs of two species of spider, Filistata hibernalis and Lycosa lenta at rest and during two min of forced activity. 2. During the first 10 to 15 s of activity, nearly all phosphagen is depleted and adenylate energy charge drops from ca. 0.9 to a value of 0.6 to 0.7. For the remainder of the two min of activity, a steady state with respect to phosphagen and adenine nucleotides is maintained (Figs. 4-7). 3. Rates of d-lactate accumulation appear to be constant or to increase after the first 10 s of activity (Fig. 3). In these spiders, the highest rates of lactate accumulation are not associated with the fastest running speeds. 4. The rapid decrease in movement that occurs over the first 10 to 20 s of activity in these and many other species of spiders may be largely related to the depletion of high-energy phosphate (∼ P): maximum rates of anaerobic and aerobic synthesis of ∼ P are several times lower than are the rates at which ∼ P is used from stores (Table 3). The large amounts of Pi released by depleting these stores would represent a potent buffer for H+ produced during lactate synthesis (Figs. 6 and 3). 5. Carbohydrate stores do not change significantly and do not appear to be the limiting factor for short (<2 min), maximum bursts of activity. 6. Spiders that lack extensive tracheal systems resemble other lunged animals physiologically and biochemically more than they resemble insects.
1.1. In the tail muscles of Crangon crangon metabolite concentrations were measured after different periods of escape swimming and subsequent recovery.2.2. Tail flipping results in a dramatic breakdown of phosphoarginine, but only little lactate is formed. As the phosphagen is depleted rapidly, the energy charge decreases and fatigue sets in.3.3. During recovery the ATP level is restored within a few minutes, phosphagen is replenished after 30 min. Large quantities of lactate accumulate which disappear very slowly.4.4. In the haemolymph lactate increases only slightly.
Article
In the two collembolan species Orchesella cincta and Tomocerus minor the water content, haemolymph osmotic pressure and transpiration rate fluctuate with the feeding rhythm during each instar. The changes in water content, however, are due to changes in dry weight, because the absolute water weight stays constant during the instar.The intake of food is probably the cause of the increase in haemolymph osmotic pressure. Increase of osmotically active substances in the blood and/or blood volume reduction may be responsible for the rise in osmotic pressure. This change in osmotic pressure in turn may affect the responsiveness of the animals to water as well as their feeding behaviour.Changes in the epicuticle and in epidermal cell membranes may cause changes in the rate of transpiration. The high rate observed during ecdysis and during the mid-instar may explain the behaviour of the animals in varied water conditions.Dehydration during the instar causes an equivalent rise in osmotic pressure for both Tomocerus minor and Orchesella cincta. The water loss appears to involve the haemolymph. The physiological state of the animal does not influence the rise in osmotic pressure. There are no signs of any osmoregulation in the two species.
Article
1. The scallopChlamys opercularis uses jet propulsion swimming as a means of escape if attacked by the star fishMarthasterias glacialis. The energy for these rapid movements is supplied by the depletion of the phosphagen phospho-L-arginine. During escape swimming the energy charge of the adductor muscle drops from 0.93 to 0.42. Due to the decrease of phospho-L-arginine from 20.4 to 1.5 mol/g fresh wt there is a concomitant increase of L-arginine from 14.7 to 34.7 mol/g fresh wt. No octopine, D- or L-lactate was accumulated in exhausted animals. 2. During the first 30 min of recovery in aerated sea water, octopine, instead of lactate, is synthesized in adductor muscles. The energy charge rises to 0.92. Within 60 min the phospho-L-arginine pool is replenished and half of the accumulated octopine again metabolized. 3. During anaerobic revovery, i.e. when the scallops are kept exposed to air, octopine synthesis is pronounced (7.5 mol/g fresh wt/h). The energy charge increases to 0.85. However, under these conditions no phospho-L-arginine is formed. 4. There is no evidence for transport of octopine from the adductor muscle to other tissues.
Article
1. The metabolism of the glycolytic end product, octopine, was investigated in vivo in the cuttlefish,Sepia officinalis. Octopine was the major mantle muscle end product produced during hypoxia, exhaustive swimming, or exhaustive swimming followed by hypoxia (muscle octopine rose from 0.2 to 3.7, 8.6, and 13.4 mol/g wet wt. respectively). Octopine concentration was inversely correlated with muscle glycogen and arginine phosphate concentrations and these substrates were almost completely depleted after swimming to exhaustion. Alanine, -glycerophosphate, pyruvate, and malate were other, minor end products. 2. Blood octopine (0.02 mol/ml at rest), pyruvate, and alanine concentrations were elevated during hypoxia and during recovery from hypoxia or exercise but not during exercise itself. Maximal blood octopine concentrations were 8-fold higher than resting levels and blood octopine appeared to be derived from the release of muscle octopine into the bloodstream. 3. 14C-A-octopine (radiolabelled in the arginine moiety: N2-(1-carboxyethyl)[U-14C]L-arginine) was administered intravenously and tissue uptake patterns showed that mantle muscle was relatively poor at the uptake of blood14C-A-octopine while brain and ventricle rapidly concentrated the compound. Parallel experiments in which [U-14C]D-glucose or [U-14C]L-arginine were administered showed that there are distinct tissue specific uptake patterns for each of the three radiolabelled compounds. 4. The tissue breakdown of14C-A-octopine taken up from the blood to form14C-arginine was found to be 0, 6, 32 and 20% respectively for mantle muscle, gill, ventricle, and brain. When delivered by specific injection into mantle muscle or brain,14C-A-octopine oxidation was 5% and 40% respectively after 20 min under resting, aerobic conditions. 5. The data indicate that while mantle muscle readily produces octopine as a glycolytic end product, the tissue has little capacity for the oxidation of octopine. Muscle octopine appears to be released into the bloodstream and can be readily taken up by other tissues. The pyruvate moiety of octopine could be oxidized as an aerobic substrate by the Krebs cycle in tissues such as brain and ventricle with the arginine moiety being recycled to the muscle. The possible existence of a modified Cori cycle, to make use of octopine as a gluconeogenic substrate, is discussed.
Article
In the flight muscle of Locusta migratoria L., arginine kinase activity increased 10-fold when 5th instar larvae and adult animals were compared. During the onset of flight, ATP decreased slightly with the amount of phospho-l-arginine remaining constant. Thus, high arginine kinase activity characterizes the adult muscle, giving rise to the speculation that the phospho-l-arginine/l-arginine kinase system does not act only as a buffer system for high-energy phosphate but also as a shuttle mechanism for high-energy phosphate between mitochondria and myofibrils. Judged from electrophoretic mobility, only one isoenzyme exists that is not bound to subcellular structures. Calculations of the diffusive fluxes of ATP, ADP, phosphate, phospho-l-arginine and l-arginine between the sites of ATP-consumption and production, respectively, can be interpreted in such a way, that the low concentration of ADPfree might limit ATP-turnover during flight. Judging from the high arginine kinase activity, the major acceptor for high-energy phosphate at the mitochondria could be l-arginine, while phospho-l-arginine is transphosphorylated to ATP at the myofibrils, thus presumably serving as an energy shuttle.
1.1. During bursts of rapid tail flipping by the yabby Cherax destructor, arginine phosphate reserves are depleted and energy charge falls before lactate starts to accumulate in the tail musculature. Regulation of anaerobic glycolysis in this muscle was investigated by examining the effects of arginine phosphate, adenylates and pH on the properties of the glycolytic enzymes phosphofructokinase, pyruvate kinase and lactate dehydrogenase.2.2. Phosphofructokinase was purified 60-fold. The enzyme was insensitive to physiological concentrations of arginine phosphate. Of the adenylates, AMP had the most marked effect by converting the fructose-6-phosphate saturation curve from sigmoidal to hyperbolic, resulting in a large decrease in Km/S0.5 fructose-6-phosphate. Enzyme activity decreased markedly below pH 7.0.3.3. Pyruvate kinase was purified 63-fold. While the properties of the enzyme were not influenced by arginine phosphate, they were strongly affected by physiological concentrations of ATP and ADP. ATP inhibition was partially removed by fructose-1,6-diphosphate.4.4. At pH values above 7.0 yabby tail muscle lactate dehydrogenase displayed properties typical of the vertebrate LDH M4 isoenzyme. However, at pH 6.5, substrate inhibition by pyruvate increased and Km pyruvate was reduced, so that the enzyme displayed properties typical of the vertebrate LDH H4 isoenzyme.5.5. It is proposed that the effects of changes in adenylate concentrations and/or pH on the properties of phosphofructokinase, pyruvate kinase and lactate dehydrogenase could be involved in regulatory glycolysis in yabby tail muscle.
Article
Procedural modifications of the luciferase method for ATP assay in conjunction with enzymatic conversion of AMP and ADP allow the assay of all three adenine nucleotides in quantities ranging from 4 to 20 pmoles. An unmodified Beckman scintillation detector at ambient temperature and in a coincidence mode of operation serves as a suitable instrument for quantitating light emitted by the enzyme preparation. The most significant modifications include use of Ca3(PO4) activated crude arsenate extracts of desiccated firefly lanterns, low arsenate concentrations during the assay, and an assay pH of 8.0. Extracts handled in this manner exhibit approximately fivefold higher activity than nonactivated extracts employed at pH 7.4 and 50 mm arsenate. Stability of activated extracts is also somewhat greater than for nonactivated preparations. ADP can be 95% enzymatically converted to ATP by treatment with phosphoenolpyruvate and pyruvate kinase under the conditions described. If myokinase is included, approximately 90% of sample AMP can be converted to ATP. Follwing the appropriate enzymatic treatment, the nucleotides are assayed as ATP and amounts calculated by comparison to curves established for known nucleotide standards. The method is appropriate for perchloric acid extracts of biological tissue and certain considerations necessary for application to experimental situations are described.
1.1. Diphosphopyridine nucleotide coenzyme-linked lactate dehydrogenases from 48 species representing six invertebrate phyla have been examined for lactate stereospecificity and starch gel electrophoretic mobility.2.2. Every organism was found to contain enzyme activity for only one lactate stereoisomer, although in several cases multiple molecular forms were observed.3.3. The minimum number of changes in stereospecificity to accommodate the evolution of the major invertebrate classes are four.4.4. An alternative evolutionary tree for the invertebrates based on lactate dehydrogenase is presented which requires only one change in stereospecificity.
Article
Arginine can be estimated spectrophotometrically by the oxidation of NADH using octopine dehydrogenase. The method is highly specific for this amino acid and is applicable to the estimation of arginine in the presence of mono- and disubstituted guanidino compounds.
Article
The lowest contents of ATP and the lowest ATP/AMP concentration ratios are observed in the molluscan muscles that have very low rates of energy expenditure during contraction. The highest contents of ATP are observed in the extremely aerobic insect flight muscle and the extremely anaerobic pectoral muscle of the pheasant and domestic fowl. In general, the lowest ATP/AMP concentration ratios are observed for muscle in which the variation in the rate of energy utilization is small (e.g. some molluscan muscles, heart muscle); the highest ratios are observed in muscles in which this variation is large (lobster abdominal muscle, pheasant pectoral muscle, some insect flight muscles). This finding is consistent with the proposed role of AMP and the adenylate kinase reaction in the regulation of glycolysis. However, in the flight muscle of the honey-bee the ATP/AMP ratio is very low, so that glycolysis may be regulated by factors other than the variation in AMP concentration. The variation in the contents of arginine phosphate in muscle from the invertebrates is much larger than the variation in creatine phosphate in muscle from the vertebrates. The contents of hexose monophosphates and pyruvate are, in general, higher in the muscles of vertebrates than in those of the invertebrates. The contents of phosphoenolpyruvate are similar in all the muscles investigated, except for the honey-bee in which it is about 4-10-fold higher. The mass-action ratios for the reactions catalysed by phosphoglucoisomerase and adenylate kinase are very similar to the equilibrium constants for these reactions. Further, the variation in the mass-action ratios between muscles is small. It is concluded that these enzymes catalyse reactions close to equilibrium. However, the mass-action ratios for the reactions catalysed by phosphofructokinase and pyruvate kinase are much smaller than the equilibrium constants. The variation in the ratios between different muscles is large. It is concluded that these enzymes catalyse nonequilibrium reactions. Since the variation in the mass-action ratios for the reactions catalysed by the phosphagen kinases (i.e. creatine and arginine phosphokinases) is small, it is suggested that these reactions are close to equilibrium.
Article
1. The maximum activities of hexokinase, phosphorylase and phosphofructokinase have been measured in extracts from a variety of muscles and they have been used to estimate the maximum rates of operation of glycolysis in muscle. These estimated rates of glycolysis are compared with those calculated for the intact muscle from such information as oxygen uptake, glycogen degradation and lactate formation. Reasonable agreement between these determinations is observed, and this suggests that such enzyme activity measurements may provide a useful method for comparative investigations into quantitative aspects of maximum glycolytic flux in muscle. 2. The enzyme activities from insect flight muscle confirm and extend much of the earlier work and indicate the type of fuel that can support insect flight. The maximum activity of hexokinase in some insect flight muscles is about tenfold higher than that in vertebrate muscles. The activity of phosphorylase is greater, in general, in vertebrate muscle (particularly white muscle) than in insect flight muscle. This is probably related to the role of glycogen breakdown in vertebrate muscle (particularly white muscle) for the provision of ATP from anaerobic glycolysis and not from complete oxidation of the glucose residues. The activity of hexokinase was found to be higher in red than in white vertebrate muscle, thus confirming and extending earlier reports. 3. The maximum activity of the mitochondrial glycerophosphate dehydrogenase was always much lower than that of the cytoplasmic enzyme, indicating that the former enzyme is rate-limiting for the glycerol 3-phosphate cycle. From the maximum activity of the mitochondrial enzyme it can be calculated that the operation of this cycle would account for the reoxidation of all the glycolytically produced NADH in insect flight muscle but it could account for only a small amount in vertebrate muscle. Other mechanisms for this NADH reoxidation in vertebrate muscle are discussed briefly.
Article
The energy charge of the adenylate system, half of the average number of anhydride-bound phosphate groups per adenine moiety, has been proposed as a metabolic regulatory parameter. For several reactions that participate in biosynthesis or other adenosine triphosphate utilizing sequences, plots of enzyme activity against energy charge have positive slopes that increase with charge; thus these curves (type U) are concave upward and steep in the region of high charge. End-product feedback inhibition of the type demonstrated for many biosynthetic regulatory enzymes must be reflected in a decrease in the slope of such curves on the addition of the end product. The area between the curve representing absence of end product and that representing a saturating level of it should indicate the operational range of the regulatory enzyme. Within this range, if either end-product concentration or energy charge is constant the enzyme will respond only to variation in the other; but it may be expected that both parameters affect the behavior of the enzyme in the intact cell. For several reactions that participate in adenosine triphosphate regenerating sequences, plots of enzyme activity against energy charge have negative slopes that increase with charge; thus these curves (type R) are concave downward and steep in the region of high charge. Such sequences also supply primary metabolic intermediates needed as starting points in biosyntheses, and in some cases have been shown to be regulated also by the concentration of one or more of these intermediates. Inhibition of this type should be reflected in an increase in the negative slope of such curves on addition of the regulatory metabolite. As in the case of type U curves, a regulatory area will exist between the curves representing zero concentration and saturating concentration of the modifying metabolite. Experimental examples of both types of pattern are provided in the following two papers. It is proposed that the overlap of such regulatory type R and type U patterns illustrates graphically some of the ways in which energy charge and the concentrations of primary intermediates and of biosynthetic end products interact to stabilize the energy charge and to adjust the partitioning of substrates among competing metabolic functions in response to changing metabolic situations in the cell.
Zur Funktionsmorphologie des Sprungapparates der Springschwänze am Beispiel von Arten der Gattung Tomocerus (Collembola, Tomoceridae)
  • Eisenbeis
Leben ohne Sauerstoff: die Rolle der anaeroben Glycolyse bei aquatischen wirbellosen Tieren
  • Gäde
Beurteilung und Kontrolle der Qualität von Meβergebnissen
  • Stähler
Applications of firefly luciferase
  • Lundin
Ökophysiologische Untersuchungen zur Anpassung der Atmung und des Energiestoffwechsels von Collembolen (Apterygota) an Sauerstoffmangel
  • Rüssbeck
Determination of the energy charge in two species of Collembola
  • Tosi
L-(+)-Lactat. Flurorimetrische Methode
  • Passoneau
The energetics of a jumping springtail, Tomocerus flavescens (Collembola)
  • Zinkler