114 High-Temperature Ecosystems Temperature Limits to Life Extreme environments were characterized earlier by the absence of species belonging to large systematic groups In thermal ecosystems, as noted earlier, not only are these large systematic groups not found, but within groups, species numbers are low, compared with cool water communities In general, in terms of temperature tolerance, there is a progression from more ‘‘primitive’’ to higher taxonomic groups, and from small to large individual size Later I consider the arguments for the evolution of the various temperature tolerance ranges What are the observed limits, based on sampling and observation of thermal ecosystems? Four different groups of organisms need to be considered: (a) the heterotrophic procaryotic bacteria, (b) the procaryotic photoautotrophs, (c) the eucaryotic microorganisms, both heterotrophic and photoautotrophic, and (d) the eucaryotic metazoans Much of the literature prior to 1978 on these limits has been summarized The study of photosynthetically active thermally tolerant organisms really began with the pioneering work of W A Setchell The main body of his work was never published, but it exists as a 215-page manuscript in the archives of the University of California at Berkeley A brief summary of the temperature limits portion of this work was published in Science Setchell reported the upper temperature for ‘‘algae’’ as 75 to 77 1C, and for bacteria to be 89 1C A later investigator claimed, on the basis of superficial samples in Yellowstone, that organisms could not grow above 73 1C, but this work relied on the uptake of radioactive phosphorous as the indicator of life; what was very likely being measured was the upper temperature for photosynthesis rather than the upper temperature for life In other older records of maximum temperatures, unfortunately, some observers confused bluegreen algae, procaryotic cyanobacteria, with green algae, eucaryotes Within the procaryotes, there has also been confusion about cyanobacteria versus filamentous bacteria Furthermore, it was not realized how steep the thermal gradient could be, thus putting a premium on temperature measurements at precisely the point where organisms are growing in the field More recently, the discovery of ocean thermal vents (discussed earlier) has reopened some of the controversy regarding these limits Heterotrophic procaryotes have colonized habitats at all temperatures up to the boiling point of water (100 1C) at sea level The most thermophilic of these organisms have not been cultured, but they are easily sampled in the parent thermal communities using glass slides and simple photomicroscopy On the basis of these findings, the prediction is that life is possible at any temperature at which there is liquid water This prediction has now been verified by the preliminary explorations of the thermal vent communities on the ocean floor (discussed earlier) with microorganisms living at temperatures far in excess of 100 1C However, reports of organisms living in water to 300 1C are still provoking argument As noted earlier, the most extremely thermophilic procaryotes have not even been cultured This may be in part due to insufficient knowledge about the nutritional requirements of these heterotrophs, but it might also be due to the difficulty of maintaining cultures near the boiling point of water The problem is exacerbated in the case of thermal vent microorganisms growing at both extreme temperatures and pressures Many of these species are also obligate anaerobes, for which even extremely low concentrations of oxygen are poisonous Others are endosymbionts, which are also notoriously difficult to culture Just getting the samples to the surface in a viable condition is a problem, and special culture techniques are required for the methanogens In summary, thermophilic heterotrophic procaryotes are apparently not limited by temperature but by the presence of liquid water At the surface this is approximately 100 1C (depending on altitude), but at depth in the ocean life is found at substantially higher temperatures, limited by suitable nutrients, pH, and energy sources The temperature limit for procaryotic photosynthetic autotrophs (both cyanobacteria and photosynthetic bacteria) is substantially below 100 1C on the surface All of the observations and experimental evidence to date suggests a maximum limit of 73 to 74 1C Of this group the most thermophilic are the photosynthetic procaryotes, of which the most temperature tolerant is the single-celled species of cyanobacterium (Synechococcus lividus) and the filamentous photosynthetic bacterium (Chloroflexus aurantiacus) These species are found in nature at temperatures up to 74 1C, although the optimum temperature is 63 to 67 1C for the cyanobacteria and even lower, about 55 1C, for the filamentous bacterium In general, the filamentous forms of the photosynthetic procaryotes seem to have adapted to much lower optimal temperatures than the single-celled forms such as Synechococcus sp Eucaryotic microorganisms are found in nature at substantially lower temperatures than are procaryotes Different reactions and responses to thermal environments are found in (a) fungi, (b) eucaryotic algae, (c) protozoa, and (d) metazoans, including invertebrates, vascular plants, and, vertebrates Fungi: In general, thermophilic and thermotolerant fungi are found at temperatures lower than 60 1C and occur at this temperature only in acid thermal waters In the very common and widespread ‘‘alkaline’’ hot spring communities, where the pH is initially somewhat acid because of dissolved carbon dioxide but rapidly rises when exposed to the air, free-living filamentous fungi are absent, even at temperatures below 40 1C There are reports of fungi parasitic on cyanobacteria that would probably be found at somewhat higher temperatures, but these have not been found in the ‘‘alkaline’’ thermal effluents of Yellowstone Park and are, in any case, poorly known (although there is a remarkable thermal range of the disease-causing fungus, Dactylaria gallopava) Single-celled and filamentous green algae as well as diatoms become abundant at temperatures around 40 1C and below Earlier reports in the literature of diatoms growing at higher temperatures relied only on the recovery of the resistant siliceous frustules, without demonstrating that the cells were alive or growing The maximum temperatures for which diatoms can be proved to be surviving and growing is 43 to 44 1C This particular diatom, Achanthes exigua, has an optimum temperature of 40 1C The single-celled and filamentous green algae have very similar temperature limits to those of the diatoms Below 40 1C in the ‘‘alkaline’’ thermal outflows of Yellowstone, the diversity of algal species rises (discussed in a later section) Although some mats of filamentous green algae