Metabolic depression in animals: physiological perspectives and biochemical generalizations

Depression of metabolic rate has been recorded for virtually all major anim al phyla in response to environmental stress. The extent of depression is u sually measured as the ratio of the depressed metabolic rate to the normal resting metabolic rate. Metabolic rate is sometimes only depressed to appro x. 80% of the resting value (i.e. a depression of approx. 20% of resting); it is more commonly 5-40 % of resting (i.e. a depression of approx. 60-95% of resting); extreme depression is to 1 % or less of resting, or even to an unmeasurably low metabolic rate (i.e. a depression of approx. 99-100 % of resting). We have examined the resting and depressed metabolic rate of anim als as a function of their body mass, corrected to a common temperature. Th is allometric approach allows ready comparison of the absolute level of bot h resting and depressed metabolic rate for various animals, and suggests th ree general patterns of metabolic depression. Firstly, metabolic depression to approx. 0.05-0.4 of rest is a common and r emarkably consistent pattern for various non-cryptobiotic animals (e.g. mol luscs, earthworms, crustaceans, fishes, amphibians, reptiles). This extent of metabolic depression is typical for dormant animals with 'intrinsic' dep ression, i.e. reduction of metabolic rate in anticipation of adverse enviro nmental conditions but without substantial changes to their ionic or osmoti c status, or state of body water. Some of these types of animal are able to survive anoxia for limited periods, and their anaerobic metabolic depressi on is also to approx. 0.05-0.4 of resting. Metabolic depression to much les s than 0.2 of resting is apparent for some 'resting', 'over-wintering' or d iapaused eggs of these animals, but this can be due to early developmental arrest so that the egg has a low 'metabolic mass' of developed tissue (comp ared to the overall mass of the egg) with no metabolic depression, rather t han having metabolic depression of the entire cell mass. A profound decreas e in metabolic rate occurs in hibernating (or aestivating) mammals and bird s during torpor, e.g. to less than 0.01 of pre-torpor metabolic rate, but t here is often no intrinsic metabolic depression in addition to that reducti on in metabolic rate due to readjustment of thermoregulatory control and a decrease in body temperature with a concommitant Q(10) effect. There may be a modest intrinsic metabolic depression for some species in shallow torpor (to approx. 0.86) and a more substantial metabolic depression for deep tor por (approx. 0.6), but any energy saving accruing from this intrinsic depre ssion is small compared to the substantial savings accrued from the readjus tment of thermoregulation and the Q(10) effect. Secondly, a more extreme pattern of metabolic depression (to < 0.05 of rest ) is evident for cryptobiotic animals. For these animals there is a profoun d change in their internal environment - for anoxybiotic animals there is a n absence of oxygen and for osmobiotic, anhydrobiotic or cryobiotic animals there is an alteration of the ionic/osmotic balance or state of body water . Some normally aerobic animals can tolerate anoxia for considerable period s, and their duration of tolerance is inversely related to their magnitude of metabolic depression; anaerobic metabolic rate can be less than 0.005 of resting. The metabolic rate of anhydrobiotic animals is often so low as to be unmeasurable, if not zero. Thus, anhydrobiosis is the ultimate strategy for eggs or other stages of the life cycle to survive extended periods of environmental stress. Thirdly, a pattern of absence of metabolism when normally hydrated (as oppo sed to anhydrobiotic or cryobiotic) is apparently unique to diapaused eggs of the brine-shrimp (Artemia spp., an anostracan crustacean) during anoxia. The apparent complete metabolic depression of anoxic yet hydrated cysts (a nd extreme metabolic depression of normoxic, hypoxic, or osmobiotic, yet hy drated cysts), is an obvious exception to the above patterns. In searching for biochemical mechanisms for metabolic depression, it is cle ar that there are five general characteristics at the molecular level of ce lls which have a depressed metabolism; a decrease in pH, the presence of la tent mRNA, a change in protein phosphorylation state, the maintenance of on e particular energy-utilizing process (ion pumping), and the down-regulatio n of another (protein synthesis). Oxygen sensing is now the focus of intens e investigation and obviously plays an important role in many aspects of ce ll biology. Recent studies show that oxygen sensing is involved in metaboli c depression and research is now being directed towards characterising the proteins and mechanisms that comprise this response. As more data accumulat e, oxygen sensing as a mechanism will probably become the sixth general cha racteristic of depressed cells. The majority of studies on these general characteristics of metabolically d epressed cells come From members of the most common group of animals that d epress metabolism, those non-cryptobiotic animals that remain hydrated and depress to 0.05-0.4 of rest. These biochemical investigations are becoming more molecular and sophistica ted, and directed towards defined processes, but as yet no complete mechani sm has been delineated, The consistency of the molecular data within this g roup of animals suggests similar metabolic strategies and mechanisms associ ated with metabolic depression. The biochemical 'adaptations' of anhydrobio tic organisms would seem to be related more to surviving the dramatic reduc tion in cell water content and its physico-chemical state, than to molecula r mechanisms for lowering metabolic rate. Metabolic depression would seem t o be an almost inevitable consequence of their altered hydration state. The unique case of profound metabolic depression of hydrated Artemia spp, c ysts under a variety of conditions could reflect unique mechanisms at the m olecular level. However, the available data are not consistent with this po ssibility (with the exception of a uniquely large decrease in ATP concentra tion of depressed, hydrated Artemia spp. cysts) and the question remains: h ow do cells of anoxic and hydrated Artemia spp. differ from anoxic goldfish or turtle cells, enabling them so much more completely to depress their me tabolism?