Biochemical ecology of deep-sea animals

Deep-sea ecosystems contain unique endemic species whose distributions show strong vertical patterning in the case of pelagic animals and sharp horizontal patterning in the case of benthic animals living in or near the deep-sea hydothermal vents. This review discusses the biochemical adaptations that enable deep-sea animals to exploit diverse deep-sea habitats and that help establish biogeographic patterning in the deep-sea. The abilities of deep-sea animals to tolerate the pressure and temperature conditions of deep-sea habitats are due to pervasive adaptations at the biochemical level: enzymes exhibit reduced perturbation of function by pressure, membranes have fluidities adapted to deep-sea pressures and temperatures, and proteins show enhanced structural stability relative to homologous proteins from cold-adapted shallow-living species. Animals from the warmest habitable regions of hydrothermal vent ecosystems have enzymes and mitochondria adapted to high pressure and relatively high temperatures. The low metabolic rates of bathypelagic fishes correlate with greatly reduced capacities for ATP turnover in locomotory muscle. Reduced light and food availability in bathypelagic regions select for low rates of energy expenditure in locomotory activity. Deep-sea animals thus reflect the importance of biochemical adaptations in establishing species distribution patterns and appropriate rates of metabolic turnover in different ecosystems.     

Pathways for oxidative fuel provision to working muscles: Ecological consequences of maximal supply limitations

The study of metabolic fuel provision and its regulation has reached an exciting stage where specific molecular events can be correlated with parameters of the organism's ecology. This paper examines substrate supply pathways from storage sites to locomotory muscle mitochondria and discusses ecological implications of the limits for maximal flux through these pathways. The relative importance of the different oxidative fuels is shown to depend on aerobic capacity. Very aerobic, endurance-adapted animals such as long distance migrants favor the use of lipids and intramuscular fuels over carbohydrates and circulatory fuels. The hypothesis of functional co-adaptation between oxygen and metabolic fuel supply systems allows us to predict that the capacity of several biochemical processes should be scaled with maximal oxygen consumption. Key enzymes, transmembrane transporter proteins, glucose precursor supply and soluble fatty acid transport proteins must all be geared to support higher maximal glucose and fatty acid fluxes in aerobic than in sedentary species.     

Pathways for oxidative fuel provision to working muscles: ecological consequences of maximal supply limitations.

The study of metabolic fuel provision and its regulation has reached an exciting stage where specific molecular events can be correlated with parameters of the organism's ecology. This paper examines substrate supply pathways from storage sites to locomotory muscle mitochondria and discusses ecological implications of the limits for maximal flux through these pathways. The relative importance of the different oxidative fuels is shown to depend on aerobic capacity. Very aerobic, endurance-adapted animals such as long distance migrants favor the use of lipids and intramuscular fuels over carbohydrates and circulatory fuels. The hypothesis of functional co-adaptation between oxygen and metabolic fuel supply systems allows us to predict that the capacity of several biochemical processes should be scaled with maximal oxygen consumption. Key enzymes, transmembrane transporter proteins, glucose precursor supply and soluble fatty acid transport proteins must all be geared to support higher maximal glucose and fatty acid fluxes in aerobic than in sedentary species.     

Review¶Psychrophilic enzymes: molecular basis of cold adaptation

Psychrophilic organisms have successfully colonized polar and alpine regions and are able to grow efficiently at sub-zero temperatures. At the enzymatic level, such organisms have to cope with the reduction of chemical reaction rates induced by low temperatures in order to maintain adequate metabolic fluxes. Thermal compensation in cold-adapted enzymes is reached through improved turnover number and catalytic efficiency. This optimization of the catalytic parameters can originate from a highly flexible structure which provides enhanced abilities to undergo conformational changes during catalysis. Thermal instability of cold-adapted enzymes is therefore regarded as a consequence of their conformational flexibility. A survey of the psychrophilic enzymes studied so far reveals only minor alterations of the primary structure when compared to mesophilic or thermophilic homologues. However, all known structural factors and weak interactions involved in protein stability are either reduced in number or modified in order to increase their flexibility.     

The biochemistry of natural fasting at its limits.

There are several groups of animals that are adapted for extremely long duration fasting as part of their reproductive cycle. Penguins, bears and seals routinely fast without food or water for months at time. However, they do not 'starve', as the biochemical implications of starving are very different from those of successful fasting. There are distinct biochemical adaptations in lipid, carbohydrate and especially protein metabolism that allow these animals to survive. It appears, at least for penguins and seals, that the duration of the fast may be limited by changes that occur in biochemical regulation near the ned of the fast. In all of these species, the biochemistry of fasting and the ecological and behavioral demands of their breeding cycles are closely interrelated.     

Molecular adaptations to cold in psychrophilic enzymes

Psychrophiles or cold-loving organisms successfully colonize cold environments of the Earth's biosphere. To cope with the reduction of chemical reaction rates induced by low temperatures, these organisms synthesize enzymes characterized by a high catalytic activity at low temperatures associated, however, with low thermal stability. Thanks to recent advances provided by X-ray crystallography, protein engineering and biophysical studies, we are beginning to understand the molecular adaptations responsible for these properties which appear to be relatively diverse. The emerging picture suggests that psychrophilic enzymes utilize an improved flexibility of the structures involved in the catalytic cycle, whereas other protein regions if not implicated in catalysis may or may not be subjected to genetic drift.     

The biochemistry of natural fasting at its limits

There are several groups of animals that are adapted for extremely long duration fasting as part of their reproductive cycle. Penguins, bears and seals routinely fast without food or water for months at time. However, they do not starve, as the biochemical implications of starving are very different from those of successful fasting. There are distinct biochemical adaptations in lipid, carbohydrate and especially protein metabolism that allow these animals to survive. It appears, at least for penguins and seals, that the duration of the fast may be limited by changes that occur in biochemical regulation near the end of the fast. In all of these species, the biochemistry of fasting and the ecological and behavioral demands of their breeding cycles are closely interrelated.     

Ultrastructure and biochemistry of the pineal organ in deep-sea lanternfishes (Myctophidae)

Pineal structural and biochemical adaptations in lanternfishes included: 1) few photoreceptor outer segment discs; 2) conventional synapses between photoreceptors and pineal neurons; and 3) low levels (0-60 pg/pineal) of serotonin compared to those (greater than 1.0 ng/pineal) in the goldfish pineal organ. These findings suggest reduced photosensory and/or neuroendocrine functions in these deep-sea fishes.     

Ultrastructure and biochemistry of the pineal organ in deep-sea lanternfishes (Myctophidae)

Summary Pineal structural and biochemical adaptations in lanternfishes included: 1) few photoreceptor outer segment discs; 2) conventional synapses between photoreceptors and pineal neurons; and 3) low levels (0–60 pg/pineal) of serotonin compared to those (>1.0 ng/pineal) in the goldfish pineal organ. These findings suggest reduced photosensory and/or neuroendocrine functions in these deep-sea fishes.     

Metabolic biochemistry and the making of a mesopelagic mammal.

Large seals such as northern and southern elephant seals and Weddell seals are able to dive for startling duration and enormous depth. The current dive duration record is 120 minutes (recorded for the southern elephant seal); the current depth record is 1.5 km (recorded for the northern elephant seal). Equally striking is the widespread observation that these seals when at sea spend close to 90% of the time submerged and often at great depth. For practical purposes, these species can be viewed as true mesopelagic animals when they are at sea. A review of current knowledge indicates that low power output but high efficiency metabolic functions of skeletal muscles coupled with inherently low (and potentially further suppressible) metabolic rates constitute strategic biochemical components in the 'making' of a mesopelagic mammal.     

Control of adenine nucleotide metabolism and glycolysis in vertebrate skeletal muscle during exercise

The turnover of adenosine triphosphate (ATP) in vertebrate skeletal muscle can increase more than a hundredfold during high-intensity exercise while the content of ATP in muscle may remain virtually unchanged. This requires that the rates of ATP hydrolysis and ATP synthesis are exactly balanced despite large fluctuations in reaction rates. ATP is regenerated initially at the expense of phosphocreatine (PCr) and then mainly through glycolysis from muscle glycogen. The increased ATP turnover in contracting muscle will cause an increase in the contents of adenosine diphosphate (ADP), adenosine monophosphate (AMP) and inorganic phosphate (P_i), metabolites that are substrates and activators of regulatory enzymes such as glycogen phosphorylase and phosphofructokinase. An intracellular metabolic feedback mechanism is thus activated by muscle contraction. How muscle metabolism is integrated in the intact body under physiological conditions is not fully understood. Common frogs are suitable experimental animals for the study of this problem because they can readily be induced to change from rest to high-intensity exercise, in the form of swimming. The changes in metabolites and effectors in gastrocnemius muscle were followed during exercise, post-exercise recovery and repeated exercise. The results suggest that glycolytic flux in muscle is modulated by signals from outside the muscle and that fructose 2,6-bisphosphate is a key signal in this process.     

Cell size of mammalian myocardia is not related to physiological demand

Morphological characteristics of myocardial ventricular myocytes have been evaluated from 5 mammalian orders with resting heart rates ranging from 51 to 475 bpm. The purpose was to determine if morphological characteristics of the myocardia are related to the functional demand imposed on the cell as represented by the resting heart rate. Cell size is a constant among mammals of different sizes which have different physiological demands. In contrast, there is more mitochondrial area and less myofibrillar area per cell in animals with rapidly beating hearts than in animals with slower heart rates. Additionally, the mean cross sectional area of individual myofibrils is 30% larger in the cow as compared to the mouse. These findings combined with our previous studies indicate that the different functional requirements of myocardia from different mammalian orders are satisfied by intracellular adaptations of both a structural and biochemical nature.     

Cell size of mammalian myocardia is not related to physiological demand

Morphological characteristics of myocardial ventricular myocytes have been evaluated from 5 mammalian orders with resting heart rates ranging from 51 to 475 bpm. The purpose was to determine if morphological characteristics of the myocardia are related to the functional demand imposed on the cell as represented by the resting heart rate. Cell size is a constant among mammals of different sizes which have different physiological demands. In contrast, there is more mitochondrial area and less myofibrillar area per cell in animals with rapidly beating hearts than in animals with slower heart rates. Additionally, the mean cross sectional area of individual myofibrils is 30% larger in the cow as compared to the mouse. These findings combined with our previous studies indicate that the different functional requirements of myocardia from different mammalian orders are satisfied by intracellular adaptations of both a structural and biochemical nature.     

Metabolic biochemistry and the making of a mesopelagic mammal

Large seals such as northern and southern elephant seals and Weddell seals are able to dive for startling duration and enormous depth. The current dive duration record is 120 minutes (recorded for the southern elephant seal); the current depth record is 1.5 km (recorded for the northern elephant seal). Equally striking is the widespread observation that these seals when at sea spend close to 90% of the time submerged and often at great depth. For practical purposes, these species can be viewed as true mesopelagic animals when they are at sea. A review of current knowledge indicates that low power output but high efficiency metabolic functions of skeletal muscles coupled with inherently low (and potentially further suppressible) metabolic rates constitute strategic biochemical components in the making of a mesopelagic mammal.     

Body size variability and water balance: A comparison between mainland and island populations ofMastomys huberti (Rodentia: Muridae) in Senegal

Generally rodents are found to be larger on islands than on the mainland. However, there are some exceptions to this rule, and the aim of this paper is to examine one of them. On the mainland of Senegal,Mastomys huberti occupies humid habitats. However, it occurs also on dry and sandy islands (Saloum delta), where its representatives are dwarf. Since water availability appeared to be the limiting factor in these islands when compared to the mainland, we studied water turnover characteristics in relation to body size, in mainland and island populations at the end of the dry season, under both field and laboratory conditions. All populations were found to be water balanced in their natural habitats. They presented similar rates of water turnover, even though island animals were subjected to stronger constraints than mainland ones. Laboratory experiments suggested that the physiological plasticity of one of the island populations may be reduced. Island populations have a higher kidney size to body weight ratio than those from the mainland. We propose that smaller size in the islands allows the maintenance of water balance with a smaller amount of water, and that a higher ratio of kidney filtration surface to body size may helpMastomys huberti to survive in dry islands. We discuss the factors responsible for body size variability and variation in water exchange characteristics and conclude that different factors could explain body size variation among island populations, depending on the species considered and the ecological constraints met within the islands.     

Psychrophilic and psychrotrophic microorganisms

Psychrophilic and psychrotrophic microorganisms have the ability to grow at 0 degree C. Psychrotrophic microorganisms have a maximum temperature for growth above 20 degrees C and are widespread in natural environments and in foods. Psychrophilic microorganisms have a maximum temperature for growth at 20 degrees C or below and are restricted to permanently cold habitats. This ability to grow at low temperature may be correlated with a lower temperature characteristic than that of the mesophiles, an increasing proportion of unsaturated fatty acids in the lipid phase of the cell membrane, which makes it more fluid, and a protein conformation functional at low temperature. The relatively low maximum temperature of growth for these microorganisms is often considered to be due to the thermolability of one or more essential cellular components, particularly enzymes, while some degradative activities are enhanced, resulting in an exhaustion of cell energy, a leakage of intracellular substances or complete lysis. Psychrotrophic microorganisms are well-known for their degradative activities in foods. Some are pathogenic or toxinogenic for man, animals or plants. However in natural microbial ecosystems psychrotrophic and psychrophilic microorganisms can play a large role in the biodegradation of organic matter during cold seasons.     

Le rôle de la prospection sous-marine autonome dans les recherches de biologie marine et d'océanographie biologique

Summary At the present time the autonomous exploration of the sea may be divided into three main fields: airScuba down to 60 m; diving saucers down to 1200 m; bathyscaph down to the greatest depths of the ocean. In the near future, theScuba with special gas mixtures, excluding nitrogen, and the underwater permanent laboratories, will open a new field for biological investigations; progress in metallurgy may also allow diving with engines, without a floating tank, down to 2000 m.The ability of the deep-sea vehicles to stop and remain at a definite depth below the surface needs further research.TheScuba is interesting for investigating the biotopes where the usual devices cannot be used from a surface vessel, for instance in submarine caves. Very special biocoenoses have been found in the totally dark parts of these caves with impoverished stocks and sometimes relict species; the sampling may be perfect both on soft and hard bottoms. With the deep-sea vehicles, investigations may be carried out on the behaviour and distribution of the bottom epifauna. The bathyscaph also allows a general view of the vertical distribution of plankton much better than using plankton samplers, because the plankton nets or pumps are always working on a discontinuous scale. Unfortunately the sampling is much more difficult, especially as far as the plankton is concerned. It is necessary that the engineers pay more attention to the biological devices; very good data have been obtained for temperature, pressure, sound-velocity, etc., but in many instances the biologist diving with a deep-sea vehicle cannot do more than look at the animals and take photographs.     

Spermatozoa: models for studying regulatory aspects of energy metabolism

Spermatozoa are highly specialized cells, and they offer advantages for studying several basic aspects of metabolic control such as the role of adenosine triphosphate-(ATP)-homeostasis for cell function, the mechanisms of fatigue and metabolic depression, the metabolic channelling through the cytoplasm and the organization and regulation of glycolytic enzymes. Spermatozoa of four species with different reproductive modes are, introduced and the first results are presented: Spermatozoa of the marine wormArenicola marina are well adapted to external fertilization in sea water with fluctuating oxygen tension: they are motile for several hours in oxygen-free sea water, even when the ATP level is dramatically reduced. Anaerobic ATP production occurs by alanine, acetate and propionate fermentation probably by the same pathways known from somatic cells of this species. Under aerobic conditions the phosphagen system might function like a shuttle for energy-rich phosphate from mitochondria to the dynein-ATPases. Storage of turkey and carp spermatozoa for several hours without exogenous substrates and oxygen results in the degradation of phosphocreatine and ATP to inorganic phosphate and adenosine monophosphate (AMP), respectively. Despite low energy charges, stored spermatozoa of both species are capable of progressive movements. In carp spermatozoa fatigue of motility is not accompanied by the dramatic acidosis one discusses as an important effect in muscle fatigue. Energy metabolism of boar spermatozoa is typically based on glycolysis consuming extracellular carbohydrates and producing lactate and protons. The sperm seem to tolerate low intracellular pH (<6.5). The lack of a phosphagen system (no energy shuttle from mitochondria to the distal dynein-ATPases) is probably compensated by a high glycolytic ATP-production in the mitochondria-free piece of the flagellum.     

Slavery in the subfamily dolichoderinae (F. Formicidae) and its ecological consequences

Summary Evidence of slave-making habits in 2 species of the subfamily Dolichoderinae has been found in arid habitats of western North America. The enslaved species are of the subfamilies Myrmicinae and Formicinae. In previously reported cases of slavery in ants, both the slave-making and enslaved species are of the subfamily Formicinae., In the 2 new cases of slavery reported here, presence of slaves of another species in a colony significantly increases the breadth of diet and/or the range of temperatures at which the colony forages.