Relationships between specialized cells, capillaries and intermediary cytofibrillary elements. XIIth note. Biological evolution of the respiratory stereotype and subsystem in invertebrates

This note presents the respiratory stereotype and subsystem in invertebrates, developing the previous notes on the emunctory stereotype and subsystem (Xth and XIth notes). As in the previous ones, Cannon's homeostasis conception and Bertlanffy's theory of systems were corroborated with Needham's theory of internal laws and of limits of organizational biological levels, and with the author's theory of biological stereotypes (Marza, Repciuc, Eskenasy, 1962). Four links of the respiratory stereotype (Rsp. Stp.) and subsystem (Rsp. SS) were distinguished. The respiratory subsystem was differentiated when, in triblastic animals, the organizational level of higher worms and of their offsprings was reached. The four links of the Rsp. Stp. are: the Ist link is represented by the oxidoreduction processes of tissue and organ cells; the IInd is the internal conveying link of O2 and CO2; the IIIrd comprises the osmotic surfaces changes and the transport of gases inwards the branchiae or lungs, and later by the water (respectively air)--blood barrier; the IVth link is formed from the structures and mechanisms of rhythmic movements which significantly increase the exchanges at the barrier level. Each link has its specific properties. The gradual evolution of each link and of the vicarious organs of gas exchange is dwelt upon, as well as the interactions between the respiratory subsystem and the other homeostasis subsystems. The theoretical interpretation of the Rsp. Stp. and Rsp. SS evolution also resorted to the theories of stabilizing selection (Schmalhausen, 1949), of canalizing selection (Waddington, 1975 and of disruptive selection (Simpson, 1953; Mayr, 1970).     

Relationships between specialized cells, capillaries and intermediary cytofibrillary elements. XVIIth Note. Biological evolution of the respiratory subsystem in Reptilia

This note continues the XIIth, XVth and XVIth ones concerning the biological evolution of the respiratory subsystem (SS.Rs.) in invertebrates, aquatic vertebrates and amphibians. Author tries to discern some of the factors involved in the passage from Amphibia to Reptilia. The lengthy evolution of embryotrophic mechanisms during this process in the light of the aromorphotic theory (A. N. Sewertsow) and the accelerating form of dyschronism (De Beer) are highlighted. The result of these changes is the formation of a large telolecithal egg endowed with all the embryotrophic reserves needed for the terrestrial evolution, for its acceleration and condensation, through the suppression of the larval stage and of metamorphosis, as well as through the appearance of some new characters. The evolution of the extraembryonic area in Amniota precursors and in Amniota and their homeothermal descendants, both oviparous and viviparous, is also discussed. The succession of respiratory organs is followed up (yolk sac, external branchiae, allantois, placenta) in the light of the organ substitution theory and of the biological stereo-type theory (Marza, Repciuc, Eskenasy).     

Submersion respiration in small diving beetles (Dytiscidae)

Some small diving beetles can survive submerged through weeks and months, because they can extract oxygen, dissolved in the water, through respiratory pores in their integument. An air flux from the outside to the inside through the respiratory pores has been demonstrated. All diving beetles capable of such pore respiration are small, but not all small diving beetles have pore respiration. With increasing size, more and more of the surface must be covered by respiratory pores to meet the increasing demand of oxygen. In running water species the pore-respiration mode is regarded as an adaptation to life in current exposed substrates, thus they avoid the risk of being swept away during frequent surface visits. In stagnant water species the pore respiration mode reduces the risk of falling victim to pelagic predators. The submersion tolerant species can switch to surface respiration, e.g. during low oxygen content. The pore respiratory mechanism is believed to be a specialised plastron. The oxygen flux through the scattered, small respiratory pore area may be enhanced by a functional thinning of the boundary layer.     

Ecological and Evolutionary Aspects of Integumentary Respiration: Body Size, Diffusion, and the Invertebrata

SYNOPSIS. Most animal phyla lack specialized respiratory surfacesand all phyla contain groups that, for some part of their lifehistory, depend entirely upon integumental diffusion of respiratorygases. Animals that are diffusion-limited, yet function aerobicallyare generally small with large surface areas and there has beenconvergence for this among all phyla including the coelomateinvertebrates. Acoelomates lack specialized respiratory structuresbut have highly modified integuments, functional specializations,and features ranging from symbioses to air gulping that compensatefor diffusion limitation. The diversity of structures functioningfor integumentary respiration is much greater among invertebratesthan vertebrates. Among the higher invertebrates with respiratorysurfaces, accessory integumentary O₂ uptake is usually 20 to50% of total respiration. The high diffusion constant of O₂in air minimizes boundary effects on gas transfer and permitslarger body size, although this is limited by dry conditions.Terrestrial annelids and flatworms, both confined to moist habitats,are larger than aquatic forms which often have accessory gills.Size differences between terrestrial forms in these two phylareflect the presence of a circulation in the annelids. Ontogenetictransitions from skin breathing to other respiratory structuresoccur among marine invertebrates and vertebrates. Vertebratesapparently exercise greater integratory control over integumentalrespiration through adjustment of ventilation and perfusion;however, it is not known if these processes occur in some invertebrates.     

Cardiac septation in heart development and evolution

The heart is one of the vital organs and is functionalized for blood circulation from its early development. Some vertebrates have altered their living environment from aquatic to terrestrial life over the course of evolution and obtained circulatory systems well adapted to their lifestyles. The morphology of the heart has been changed together with the acquisition of a sophisticated respiratory organ, the lung. Adaptation to a terrestrial environment requires the coordination of heart and lung development due to the intake of oxygen from the air and the production of the large amount of energy needed for terrestrial life. Therefore, vertebrates developed pulmonary circulation and a septated heart (four-chambered heart) with venous and arterial blood completely separated. In this review, we summarize how vertebrates change the structures and functions of their circulatory systems according to environmental changes.     

Silicon metabolism in diatoms. III. Respiration and silicon uptake in Navicula pelliculosa

1. Evidence is presented that silicon uptake in the diatom Navicula pelliculosa is linked with aerobic respiration. 2. Cyanide, fluoride, iodoacetate, arsenite, azide, and fluoroacetate, at concentrations inhibitory to respiration, were also inhibitory to silicon uptake. 3. 2,4-Dinitrophenol (1 to 2 x 10(-5)M) stimulated respiration by 100 per cent, but almost completely inhibited silicon uptake. 4. The respiratory quotient of non-Si-deficient cells decreased from 0.93 to 0.75 after 4 days of starvation in darkness. Glucose (1 per cent) raised the respiratory quotient of such starved cells to 1.05. 5. Silicate (20 mg. Si/liter) stimulated respiration of unstarved Si-deficient cells by about 40 per cent. The effect of silicate on the respiration of Si-deficient cells which had been starved in darkness for 4 days was less marked. 6. The respiratory quotient of Si-deficient cells decreased from 0.8-0.9 to 0.3 after 4 days of starvation in darkness. The addition of silicate to starved cells raised the quotient to 0.5. This represented a 25 per cent stimulation of oxygen uptake concomitant with a 90 per cent stimulation of carbon dioxide evolution. 7. Glucose (1 per cent) caused an increase of respiratory quotient in starved cells from 0.3 to 0.7-0.8. The addition of silicate had no effect on the R.Q. during the oxidation of exogenous glucose. 8. Substrates (glucose, fructose, galactose, lactate, succinate, citrate, glycerol), which caused a stimulation of respiration in starved cells, also stimulated silicon uptake by those cells. However, the stimulation of silicon uptake (50 to 100 per cent) was not proportional to the respiratory stimulation by these substrates (30 to 300 per cent).     

Low community photosynthetic quotient in coral reef sediments

Fluxes of dissolved inorganic carbon and oxygen at the water-sediment interface were measured at eight coral reef stations (Indian Ocean) in summer and winter. The dark fluxes provided the community respiratory quotient (CRQ = dissolved inorganic carbon release / oxygen uptake) and the diurnal fluxes corrected from the dark fluxes gave the community photosynthetic quotient (CPQ = oxygen gross release / dissolved inorganic carbon gross uptake). The CRQ and the winter CPQ were not significantly different from 1. Summer CPQ (0.79; SD 0.02) was significantly lower than 1 due to the combined effect of the daily evolution of the community respiration and the discrepancy between the daily evolution in community oxygen respiration and community carbon respiration. These results highlight the importance of measuring simultaneously the benthic community production and respiration for long term integrated data sets, instead of the traditional daily or seasonal budget calculations from limited measures of community respiration. To cite this article: D. Taddei et al., C. R. Biologies 331 (2008).     

Oxygen uptake capacity of the amphibious fish - Amphipnous cuchia (Ham) (Symbranchiformes, Amphipnoidae)

The O2 uptake capacity of Amphipnous cuchia has been determined in relation to standard temperature of 25 degrees C. The measurement of O2 uptake indicates nearly 75% of the oxygen demand to be met through the air breathing organs and 25% by the skin and vestigeal gill through water in a normal habitat. The total VO2 during aerial-aquatic gas exchange is 60.5 ml/kg/hr. The prevention of surfacing resulted in a lower O2 uptake rate (38.29 ml/kg/hr). During submergence, the utilisation of air sacs for extracting O2 by regular pumping of water in and out is peculiar to the fish. Under normal respiratory conditions (air + water), the slope for O2 uptake through air is 0.72, 0.23 for water and 0.57 for both air + water. The average ratio borne by the fish for aquatic/air breathing (ml/kg/min) is higher in fishes below 60 g body weight, and aquatic respiration predominates in fishes weighing less than 6.0 g.     

Respiratory responses to short term hypoxia in the snapping turtle, Chelydra serpentina

Among vertebrates, turtles are able to tolerate exceptionally low oxygen tensions. We have investigated the compensatory mechanisms that regulate respiration and blood oxygen transport in snapping turtles during short exposure to hypoxia. Snapping turtles started to hyperventilate when oxygen levels dropped below 10% O(2). Total ventilation increased 1.75-fold, essentially related to an increase in respiration frequency. During normoxia, respiration occurred in bouts of four to five breaths, whereas at 5% O(2), the ventilation pattern was more regular with breathing bouts consisting of a single breath. The increase in the heart rate between breaths during hypoxia suggests that a high pulmonary blood flow may be maintained during non-ventilatory periods to improve arterial blood oxygenation. After 4 days of hypoxia at 5% O(2), hematocrit, hemoglobin concentration and multiplicity and intraerythrocytic organic phosphate concentration remained unaltered. Accordingly, oxygen binding curves at constant P(CO(2)) showed no changes in oxygen affinity and cooperativity. However, blood pH increased significantly from 7.50+/-0.05 under normoxia to 7.72+/-0.03 under hypoxia. The respiratory alkalosis will produce a pronounced in vivo left-shift of the blood oxygen dissociation curve due to the large Bohr effect and this is shown to be critical for arterial oxygen saturation.     

A functional analysis of the shift from gill- to lung-breathing during the evolution of land crabs (Crustacea, Decapoda)

The evolution of air-breathing in land crabs is associated with a progressive shift in the primary site of respiratory gas exchange from the diffusion-limited gills used for water-breathing, via a simple 'cutaneous' lung surface to the perfusion-limited, invaginated lung described in the mountain crab, Pseudothelphusa garmani. The reduced diffusion limitation over the lungs facilitates oxygen transfer from air to the tissues at lower ventilation rates but is associated with accumulation of carbon dioxide. A potential respiratory acidosis is buffered by the respiratory pigment haemocyanin and by elevation of haemolymph bicarbonate levels. These changes parallel those described in vertebrates but air-breathing crustaceans maintain relatively low carbon dioxide levels in the haemolymph, either by retaining an aquatic route for its elimination over the reduced gills or by blowing it off across the lung. Maintenance of low carbon dioxide levels may be associated with a limited capacity to buffer against an acidosis due to low levels of circulating haemocyanin (i.e. crustaceans lack red blood cells). This may ultimately limit their survival in air as an acidosis will reduce oxygen transport due to a marked Bohr effect on haemocyanin. The primary role of an invaginated lung may be to reduce rates of water loss in air.     

Determination of the respiration kinetics for mycelial pellets of Phanerochaete chrysosporium.

In mycelial pellet cultures of the white rot basidiomycete Phanerochaete chrysosporium, low oxygen concentration negatively affects the production of the extracellular lignin peroxidases and manganese peroxidases which are key components of the lignin-degrading system of this organism. To test the hypothesis that oxygen limitation in the pellets is responsible for this effect, oxygen microelectrodes were used to determine oxygen concentration gradients within the mycelial pellets of P. chrysosporium. Pellets were removed from oxygenated cultures, allowed to equilibrate with air, and probed with oxygen microelectrodes. The oxygen profiles were modelled assuming that O2 uptake follows a Michaelis-Menten relationship. The Vmax and Km values for oxygen uptake were 0.76 +/- 0.10 g/m3 of pellet per s and 0.5 +/- 0.3 g/m3, respectively. These kinetic values were used to predict respiration rates in air-flushed cultures, oxygen-flushed cultures, and cultures with large pellets (diameter greater than 6 mm). The predicted respiration rates were independently validated by experimentally measuring the evolution of carbon dioxide from whole cultures.     

Determination of the respiration kinetics for mycelial pellets of Phanerochaete chrysosporium.

In mycelial pellet cultures of the white rot basidiomycete Phanerochaete chrysosporium, low oxygen concentration negatively affects the production of the extracellular lignin peroxidases and manganese peroxidases which are key components of the lignin-degrading system of this organism. To test the hypothesis that oxygen limitation in the pellets is responsible for this effect, oxygen microelectrodes were used to determine oxygen concentration gradients within the mycelial pellets of P. chrysosporium. Pellets were removed from oxygenated cultures, allowed to equilibrate with air, and probed with oxygen microelectrodes. The oxygen profiles were modelled assuming that O2 uptake follows a Michaelis-Menten relationship. The Vmax and Km values for oxygen uptake were 0.76 +/- 0.10 g/m3 of pellet per s and 0.5 +/- 0.3 g/m3, respectively. These kinetic values were used to predict respiration rates in air-flushed cultures, oxygen-flushed cultures, and cultures with large pellets (diameter greater than 6 mm). The predicted respiration rates were independently validated by experimentally measuring the evolution of carbon dioxide from whole cultures.     

Free oxygen and evolutionary progress.

A conception of the origin of multicellularity and respiration is presented. It is assumed that the evolution of aerobic life was a phased process. The most important milestones of the process were the appearance, at first, of aerotolerance factors (catalase, peroxidase, Superoxide dismutase), and later, of an aerobic-type energy system (respiratory chain). The consecutive steps of morphophysiological progress are associated with the origin of these enzymes and enzyme systems. The advent of catalase could have given rise to the phenomenon of multicellularity on the basis of complementation of the catalase containing (deprived of another, initial enzyme, essential for the survival of cells) and catalase non-containing (preserving this initial “wild” enzyme) cells. The presence of catalase in multicellular heterotrophic fermenters led to their acquisition of photosynthesizing symbionts—protoplastids (which did not have their own catalase). The occurrence of energetically or physiologically expedient reactions in aerotolerant organisms utilizing free oxygen, did not balance the global effects of photosynthesis (an excessive accumulation of organic matter and oxygen, and a shortage of carbon dioxide). An equilibrium between organic synthesis and destruction processes was restored in the biosphere after the emergence of phosphorylative respiration. The great resemblance of enzyme systems and phosphorylation mechanisms in photosynthesis and respiration suggests that the respiratory assemblies were not created by nature anew, but evolved by way of inversion of the photosynthesizing apparatus in a part of protoplastids which had lost their capacity for photosynthesis (because of the termination of the supply of the radiant energy). The complication of the symbiosis of heterotrophs and photosynthesizers by the rise of a “third element”—protomitochondria —opened up new opportunities, the use of which could have led to a great diversification of cellular forms and thus promoted evolutionary progress.     

Entamoeba histolytica. I. Aerobic metabolism

The respiration of intact trophozoites harvested from axenic cultures of Entamoeba histolytica was studied with the polarographic technique utilizing the Clark oxygen electrode. A typical Q_o2 value for the freshly harvested amebae was 1 μatom oxygen/mg protein/hr.It was conclusively demonstrated that this parasite, a putative anaerobe, not only consumes oxygen when provided, but has a high affinity for the gas.Added glucose, galactose, and ethanol increased the respiratory rates, whereas other carbohydrates were without effect on the endogenous respiration. Intermediates of the tricarboxylic acid cycle, amino and fatty acids did not stimulate the respiration of E. histolytica.Inhibitors of the mammalian respiratory chain (cyanide, antimycin) as well as agents that inhibit enzymes catalyzing the tricarboxylic acid cycle (malonate, fluoropyruvate, fluoroacetate, fluorocitrate) had little effect on the endogenous or glucose-supported respiration. Alkylating agents (iodoacetamide, iodoacetate), cinnamate, and N-ethylymaleimide strongly inhibited the oxygen consumption of E. histolytica. The chemotherapeutic agents, Paromomycin, Emetine and Metronidazole, at concentrations that inhibit growth in vitro, did not restrict the respiration.Storage of the trophozoites at 4 C led to progressive deterioraion of the parasites and loss of endogenous and glucose-supported respiration. The deterioration was paralled by loss of SH-materials from the amebae. Likewise, sonication or lysis with detergents abolished both the endogenous respiration and response to glucose.Exogenous NADH or NADPH evoked only marginal increases in oxygen consumption of the freshly harvested amebae, but were effective respiratory substrates with stored or sonicated organisms. Addition of vitamin K₃ greatly enhanced the endogenous and glucose-supported respiration of the intact amebae, as well as enhancing the response of stored or sonicated amebae to reduced pyridine nucleotides.     

Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone

Among the air-breathing vertebrates, the avian respiratory apparatus, the lung-air sac system, is the most structurally complex and functionally efficient. After intricate morphogenesis, elaborate pulmonary vascular and airway (bronchial) architectures are formed. The crosscurrent, countercurrent, and multicapillary serial arterialization systems represent outstanding operational designs. The arrangement between the conduits of air and blood allows the respiratory media to be transported optimally in adequate measures and rates and to be exposed to each other over an extensive respiratory surface while separated by an extremely thin blood-gas barrier. As a consequence, the diffusing capacity (conductance) of the avian lung for oxygen is remarkably efficient. The foremost adaptive refinements are: (1) rigidity of the lung which allows intense subdivision of the exchange tissue (parenchyma) leading to formation of very small terminal respiratory units and consequently a vast respiratory surface; (2) a thin blood-gas barrier enabled by confinement of the pneumocytes (especially the type II cells) and the connective tissue elements to the atria and infundibulae, i.e. away from the respiratory surface of the air capillaries; (3) physical separation (uncoupling) of the lung (the gas exchanger) from the air sacs (the mechanical ventilators), permitting continuous and unidirectional ventilation of the lung. Among others, these features have created an incredibly efficient gas exchanger that supports the highly aerobic lifestyles and great metabolic capacities characteristic of birds. Interestingly, despite remarkable morphological heterogeneity in the gas exchangers of extant vertebrates at maturity, the processes involved in their formation and development are very similar. Transformation of one lung type to another is clearly conceivable, especially at lower levels of specialization. The crocodilian (reptilian) multicameral lung type represents a Bauplan from which the respiratory organs of nonavian theropod dinosaurs and the lung-air sac system of birds appear to have evolved. However, many fundamental aspects of the evolution, development, and even the structure and function of the avian respiratory system still remain uncertain.     

Similar nature of inhibition of mitochondrial respiration of heart tissue and malignant cells by methylglyoxal. A vital clue to understand the biochemical basis of malignancy

The effect of methylglyoxal on the oxygen consumption of mitochondria of heart and of several other organs of normal animals of different species has been tested. The results indicate that methylglyoxal (3.5 mM) strongly inhibits ADP-stimulated -oxoglutarate and malate plus pyruvate-dependent respiration of exclusively heart mitochondria of normal animals of different species. Whereas, with the same substrates, but at a higher concentration of methylglyoxal (7.5 mM), the respiration of mitochondria of other organs of normal animals is not inhibited. Methylglyoxal also inhibits the respiration of slices of rat and toad hearts. But this inhibition is less pronounced. However, methylglyoxal (15 mM) fails to have any effect on perfused toad heart. Using rat heart mitochondria as a model, the effect of methylglyoxal on the oxygen consumption was also tested with different respiratory substrates, electron donors at different segments of the mitochondrial respiratory chain and site-spe inhibitors to identify the specific respiratory complex which might be involved in the inhibitory effect of methylglyoxal. The results strongly suggest that methylglyoxal inhibits the electron flow through complex I of rat heart mitochondrial respiratory chain. Moreover, lactaldehyde (0.6 mM), a catabolite of methylglyoxal, can exert a protective effect on the inhibition of rat heart mitochondrial respiration by methylglyoxal (2.5 mM). The effect of methylglyoxal on heart mitochondria as described in the present paper is strikingly similar to the results of our previous work with mitochondria of Ehrlich ascites carcinoma cells and leukemic leukocytes. We have recently proposed a new hypothesis on cancer which suggests that excessive ATP formation in cells may lead to malignancy. The above mentioned similarity apparently provides a solid experimental foundation for the proposed hypothesis which has been discussed.     

Effect of hypercapnia on thermoregulation at high ambient temperature

The reported investigations were carried out on rabbits exposed for three hours to ambient temperature of 25 degrees C or 35 degrees breathing athmospheric air (controls) or gas mixtures containing 4% or 7% of CO2. During the exposure to 35 degrees C in rabbits breathing the gas mixture with 7% of CO2 the rise of rectal temperature was significantly greater, heat elimination from the auricular surface was increased, whereas the oxygen uptake was increased insignificantly. In tracheostomized rabbits breathing the gas mixture with 7% of CO2 at 32 degrees C the respiratory rate decreased but the respiration volume increased as compared with the animals breathing atmospheric air. It seems that the hyperthermic effect of hypercapnia demonstrated in this work can be attributed to the impairment of heat elimination through the upper airways due to an inhibition of thermal panting.     

Effect of oxygen concentration on photosynthesis and respiration in two hypersaline microbial mats

The effects of oxygen concentration on photosynthesis and respiration in two hypersaline cyanobacterial mats were investigated. Experiments were carried out on mats from Eilat, Israel, with moderate photosynthetic activity, and mats from Mallorca, Spain, with high photosynthetic activity. The oxygen concentration in the overlying water above the mats was increased stepwise from 0% to 100% O2. Subsequent changes in oxygen concentration, gross photosynthetic rates, and pH values inside the mats were measured with microelectrodes. According to published reports on the regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), the key enzyme in the CO2-fixation pathway of phototrophs, we expected photosynthetic activity to decrease with increasing oxygen concentration. Gross photosynthetic and total respiration rates in both mats were highest when the O2 concentration was at 0% in the overlying water. Net oxygen production rates under these conditions were the same as under air saturation (21% O2), while gross photosynthetic and respiration rates were lowest at air saturation. In both mats, gross photosynthetic and respiration rates increased upon gradually increasing the oxygen concentration in the overlying water from 21% to 100%. These results contradict the expectation that photosynthesis decreases with increasing oxygen concentration. Increased photosynthetic rates at oxygen concentrations above 21% were probably caused by enhanced oxidation of organic matter and concomitant CO2 production due to the increased oxygen availability. The cause of the high respiration rates at 0% O2 in the overlying water was presumably the enhanced excretion of photosynthetic products during increased photosynthesis. We conclude that the effect of the O2/CO2 concentration ratio on the activity of Rubisco as demonstrated in vitro on enzyme extracts cannot be extrapolated to the situation in intact microbial mats, because the close coupling of the activity of primary producers and heterotrophic bacteria plays a major role in this ecosystem.     

Neuroglobin and cytoglobin: genes, proteins and evolution

Hemoglobin and myoglobin are oxygen transport and storage proteins of most vertebrates. Neuroglobin (Ngb) and cytoglobin (Cygb)--two recent additions to the vertebrate globin superfamily--have still disputed functions. Combining the data from all available resources, we investigate the evolution of these novel globins. Both Ngb and Cygb show little sequence variation in vertebrate evolution, suggesting conserved structures and functions, and an important role in the animal's metabolism. Exon-intron patterns remained unchanged in Ngb and Cygb, with the exception of the addition of a 3' exon to Cygb early in mammalian evolution. In phylogenetic analyses, Ngb forms a common branch with globin X, another recently identified globin with undefined function in lower vertebrates, and with some invertebrate nerve globins. This shows an early divergence of this branch in animal evolution. Cygb is related to myoglobin, and associated with an eye-specific globin from birds. The pattern of globin evolution shows that proteins with clear respiratory roles evolved independently from intracellular globins with uncertain functions. This result suggests either multiple independent functional changes or a yet undefined respiratory role of tissue globins like Ngb and Cygb.