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Thermophilic Blue-Green Algae and the Thermal Environment RICHARD W

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Thermophilic Blue-Green Algae and the Thermal Environment RICHARD W BACTERIOLOGICAL REVIEWS, Dec. 1969, p. 476-504 Vol. 33, No. 4 Copyright @ 1969 American Society for Microbiology Printed Ln U.S.A. Thermophilic Blue-Green Algae and the Thermal Environment RICHARD W. CASTENHOLZ Department of Biology, University of Oregon, Eugene, Oregon 97403 INTRODUCTION.................................................. 476 DISTRIBUTION OF THERMAL WATERS.................................... 481 SOLUTES OF THERMAL WATERS .......................................... 482 DISTRIBUTION OF SPECD DS ............................................... 486 Upper and Lower Temperature LLmts.......................................... 486 Clas tion and Geographical Distribution ..................................... 487 Problems of Survival and Transport............................................ 488 STUDIES OF NATURAL POPULATIONS .................................... 489 Mat Formation and Stability.................................................. 489 Movements of Filaments and Mats ............................................. 491 Measurements of Photosynthesis and Growth .................................... 491 CULTIVATION OF THERMOPHILIC CYANOPHYTES ....................... 493 Medium and Nutrition ................................................... 493 Isolation and Maintenance................................................... 494 Rates of Growth, Photosynthesis, and Respiration in Culture....................... 495 RESPONSES TO TEMPERATURE AND LIGHT INTENSITY.................. 497 Optimal Temperature and Light Intensity....................................... 497 Effects of Light and Temperature on Pigmentation ............................... 498 Growth and Survival at Suboptimal Temperatures ................................ 499 LITERATURE CITED........................................................ 500 INTRODUCTION most striking effects, the promotion of blue-green The blue-green algae (cyanophyta) are con- algal growth (164). It is probable that habitats sidered to be thermophilic (in this review) when suitable for thermophilic organisms are going to part or all of their optimal growth temperature increase substantially. range is above 45 C. Different definitions are used Most thermal habitats are aquatic, and the for thermophily in bacteria, fungi, and animals. source of heat is telluric for nearly all of these. A maximal growth rate at temperatures over 45 C Nevertheless, insolation can raise the temperature is mainly a characteristic of procaryotic or- sufficiently in a few situations and the self-heating ganisms. Only a few species of eucaryotic protists of organic materials (thermogenesis) may bring or animals tolerate temperatures above this localized temperature to the point of ignition. (Table 1). In the range between 50 and 60 C, there Hot springs and their drainways provide the are a few fungi and the eucaryotic alga of acid most abundant aquatic habitats for thermophilic waters, Cyanidium caldarium. Photosynthetic blue-green algae. It will be these natural environ- blue-green algae are known to grow at constant ments and these blue-green algae that are dis- temperatures as high as 73 to 74 C (29), and cussed through the remainder of this paper. nonphotosynthetic bacteria as high as 95 C (26, However, the other (rarer) thermal habitats Table 1). Even many species of blue-green algae require a brief description, even though little is of nonthermal habitats have higher temperature known of their organisms in situ. Temperatures in optima than the eucaryotic algae of the same excess of 50 C may be attained in a few truly waters (79). Because of this, blue-green algae may aquatic situations solely from insolation. The be enriched for by incubating samples in light and monimolimnion (bottom waters) of a few small nonselective mineral medium at 35 C (11). meromictic saline ponds and lakes may be heated Blue-green algae are becoming more con- (to >50 C) during the seasons of high light spicuous in this age of increasing environmental intensity and retain fairly high temperatures pollution. In nutrient-enriched waters, blooms of throughout the year, since circulation of the bot- planktonic blue-green algae are more frequent, tom water is completely lacking (15, 95). Con- denser, and longer lasting (80). Similarly, thermal siderably higher temperatures (90 to 95 C) were pollution from the water coolant of power plants reached in artificial solar ponds at the Negev (nuclear and conventional) has, as one of its Institute in Israel (J. Schechter, personal com- 476 VOL. 33, 1969 THERMOPHILIC BLUE-GREEN ALGAE 477 TABLE 1. Organisms that live in hot springs at isolations of these organisms can easily be made temperatures above 45 Ca from hot springs (134) and a variety of non- Organism Temp thermal habitats such as soil, sand, air, seawater, and snow (5). Filamentous and unicellular bacteria Although the source waters of hot springs are [mainly heterotrophic ? (26, 29, 32) ] ...... 95 C usually quite low in dissolved organic compounds, Acidophilic thiobacilli (34) ......... about 60 C there are obviously a number of heterotrophic Photosynthetic (purple sulfur) bac- bacteria associated with the photosynthetic blue- teria (unpublished data) ........... 57 to 60 C green algae on which they probably depend for Photosynthetic blue-green algae (31, 38, carbon-energy sources. Some of these are fila- 146) ............. .............. 74 C mentous flexibacteria; others are nonsporeform- Cyanidium [(acidophilic) (16, 34)]. .. 56 to 57 C Fungi [(?) in hot springs (58)] ............ 60 C ing filaments or rods of other types (42). How- Diatoms (120, 169; R. P. Sheridan, personal ever, in many hot springs in Yellowstone (26) communication) ......................... 50 C and Oregon (unpublished data) there are bacteria Green algae (120, 139, 169) ............... 48 C growing above 90 C where no endogenous photo- Ciliata (45) ............................ 50 C synthetic organisms are present to support Rotifera (45) ............................ 45 C heterotrophic growth. Either the rapid flow of Ostracoda [crustacea (45; Castenholz, spring gyater (containing a minute quantity of unpublished data)] ......... ........ 49 to 50 C organic matter) is sufficient to sustain growth or Acarina [arachnida (45, 46)] ........ 50 to 51 C Diptera [larvae (28, 45, 46, 175) ] ............ 50 C these bacteria are autotrophs of some type. Coleoptera [larvae (45)] .................. 45 C Blue-green algae are particularly concentrated in hot-spring waters with a pH of over 6 where a Approximate highest constant temperatures they form conspicuous and often unialgal matlike at which they occur or at which growth has been covers over submerged substrates. Since there is demonstrated are indicated. Selected references in many hot springs a surface effluent with a on temperature limits are given for each group of thermal gradient ranging from supraoptimal to organisms. Except for Cyanidium and certain bacteria and fungi, all of the organisms occur ambient air temperature, specific differences in mainly in waters ofpH above 6. growth temperature optima may result in distinct species bands covering different portions of the gradient (Fig. 1). Since the component organisms munication). In these, meromixis was established differ in their amounts of chlorophyll-a, bilipro- by artificially increasing the salt concentration teins, and carotenoid pigments, these bands may towards the bottom. Small freshwater or saline be quite different in color, but ranging from a dark pools in warm desert or tropical island environ- brown to a yellow or rich green or blue-green. ments sometimes exceed 40 C (B. Whitton, The orange or flesh color of many hot spring mats personal communication), although air tempera- is often caused by compact masses of hetero- ture is also important in such circumstances. The trophic, carotenoid-containing, filamentous bac- origin of heat in the deep, hot brines of the Red teria. Although these generally form gelatinous Sea is telluric, and only bacterial life has been layers (sometimes a few centimeters thick) under- reported to date (174). Blue-green algae are the neath a top cover of photosynthetic blue-green principal inhabitants of alternately moist and dry algae, they are sometimes exposed over wide cliffs in most mountainous regions of the world. areas (Fig. 1, 2). In some springs, pink to red The conspicuous dark streaks of blue-green algae layers of photosynthetic purple sulfur bacteria may be heated by sun and air to temperatures of occur directly under the algal cover. over 40 C (109), but it is not known that Because of the shallowness and the clarity of growth occurs during such periods. most thermal waters, and the exposure of many Hot springs and most solar-heated aquatic hot springs to high light intensities, various types environments are composed of mineral waters, of "sun adaptation" have occurred in many whereas the environment in self-heating piles of thermophilic organisms. Laboratory and field vegetation is richly organic. Thermophilic fungi, studies of this have added an interesting dimen- sporeforming bacteria, and actinomycetes appear sion to studies of adaptation to high temperature. to be the main agents of thermogenesis in ac- In addition, the organisms of many hot springs cumulations of hay, compost, peat, and manure. have adapted to high salinity or to high concentra- A few of the fungi are active between 50 and tions of certain ions. Being partly of magmatic 60 C, whereas some of the bacteria are active to origin, most
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