Life at high temperatures

Perhaps the most important thing about dangerously high temperatures is that, for a given organism, they usually lie only a few degrees above the metabolic optimum. This is largely an unavoidable consequence of the physicochemical properties of most enzymes (Wharton, 2002). High temperatures may be dangerous because they lead to the inactivation or even the denaturation of enzymes, but they may also have damaging indirect effects by leading to dehydration. All terrestrial organisms need to conserve water, and at high temperatures the rate of water loss by evaporation can be lethal, but they are caught between the devil and the deep blue sea because evaporation is an important means of reducing body temperature. If surfaces are protected from evaporation (e.g. by closing stomata in plants or spiracles in insects) the organisms may be killed by too high a body temperature, but if their surfaces are not protected they may die of desiccation.

Death Valley, California, in the summer, is probably the hottest place on earth in which higher plants make active growth. Air temperatures during the daytime may approach 50°C and soil surface temperatures may be very much higher. The perennial plant, desert honeysweet (Tidestromia oblongifolia), grows vigorously in such an environment despite the fact that its leaves are killed if they reach the same temperature as the air. Very rapid transpiration keeps the temperature of the leaves at 40-45°C, and in this range they are capable of extremely rapid photosynthesis (Berry & Bjorkman, 1980).

Most of the plant species that live in very hot environments suffer severe shortage of water and are therefore unable to use the latent heat of evaporation of water to keep leaf temperatures down. This is especially the case in desert succulents in which water loss is minimized by a low surface to volume ratio and a low frequency of stomata. In such plants the risk of overheating may be reduced by spines (which shade the surface of a cactus) or hairs or waxes (which reflect a high proportion of the incident radiation). Nevertheless, such species experience and tolerate temperatures in their tissues of more than 60°C when the air temperature is above 40°C (Smith et al., 1984).

Fires are responsible for the highest temperatures that organisms face on earth and, before the fire-raising activities of humans, were caused mainly by lightning strikes. The recurrent risk of fire has shaped the species composition of arid and semiarid woodlands in many parts of the world. All plants are damaged by burning but it is the remarkable powers of regrowth from protected meristems on shoots and seeds that allow a specialized subset of species to recover from damage and form characteristic fire floras (see, for example, Hodgkinson, 1992).

Decomposing organic matter in heaps of farmyard manure, compost heaps and damp hay may reach very high temperatures. Stacks of damp hay are heated to temperatures of 50-60°C by the metabolism of fungi such as Aspergillus fumigatus, carried further to approximately 65°C by other thermophilic fungi such as Mucor pusillus and then a little further by bacteria and actinomycetes. Biological activity stops well short of 100°C but autocombustible products are formed that cause further heating, drive off water and may even result in fire. Another hot environment is that of natural hot springs and in these the microbe Thermus aquaticus grows at temperatures of 67°C and tolerates temperatures up to 79 °C. This organism has also been isolated from domestic hot water systems. Many (perhaps all) of the extremely thermophilic species are prokaryotes. In environments with very high temperatures the communities contain few species. In general, animals and plants are the most sensitive to heat followed by fungi, and in turn by bacteria, actinomycetes and archaebacteria. This is essentially the same order as is found in response to many other extreme conditions, such as low temperature, salinity, metal toxicity and desiccation.

An ecologically very remarkable hot environment was first described only towards the end of the last century. In 1979, a deep oceanic site was discovered in the eastern Pacific at which fluids at high temperatures ('smokers') were vented from the sea floor forming thin-walled 'chimneys' of mineral materials. Since that time many more vent sites have been discovered at mid-ocean crests in both the Atlantic and Pacific Oceans. They lie 2000-4000 m below sea level at pressures of 200-400 bars (20-40 MPa). The boiling point of water is raised to 370°C at 200 bars and to 404°C at 400 bars. The superheated fluid emerges from the chimneys at temperatures as high as 350°C, and as it cools to the temperature of seawater at about 2°C it provides a continuum of environments at intermediate temperatures.

Environments at such extreme pressures and temperatures are obviously extraordinarily difficult to study in situ and in most respects impossible to maintain in the laboratory. Some thermophilic bacteria collected from vents have been cultured successfully at 100°C at only slightly above normal barometric pressures (Jannasch & Mottl, 1985), but there is much circumstantial evidence that some microbial activity occurs at much higher temperatures and may form the energy resource for the warm water communities outside the vents. For example, particulate DNA has been found in samples taken from within the 'smokers' at concentrations that point to intact bacteria being present at temperatures very much higher than those conventionally thought to place limits on life (Baross & Deming, 1995).

There is a rich eukaryotic fauna in the local neighborhood of vents that is quite atypical of the deep oceans in general. At one vent in Middle Valley, Northeast Pacific, surveyed photographically and by video, at least 55 taxa were documented of which 15 were new or probably new species (Juniper et al., 1992). There can be few environments in which so complex and specialized a community depends on so localized a special condition. The high temperature and water loss thermal vents and other hot environments closest known vents with similar conditions are 2500 km distant. Such communities add a further list to the planet's record of species richness. They present tantalizing problems in evolution and daunting problems for the technology needed to observe, record and study them.

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