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The Thermo- Acidophilic Cyanidiophyceae (Cyanidiales)” Biodata of Valérie Reeb and Debashish Bhattacharya, authors of “The Thermo- acidophilic Cyanidiophyceae (Cyanidiales)” Dr. Valérie Reeb is currently a Postdoctoral Research Associate at the Department of Biological Science in the University of Iowa, USA. She obtained her Ph.D. from Duke University in 2005 and continued her postdoctoral studies at Duke University and the University of Iowa. Dr. Reeb’s scientific interests are in the areas of evolution of algae, protists and fungi, and molecular phylogeny of Cyanidiales (red Algae) and lichen forming-fungi. E-mail: valerie-reeb @ uiowa.edu Dr. Debashish Bhattacharya is currently a Professor in the Department of Ecology, Evolution and Natural Resources at Rutgers University. He obtained his Ph.D. from Simon Fraser University, Burnaby, Canada under the supervision of Prof. Louis Druehl. The Bhattacharya lab has broad interests in algal evolution, endosymbiosis, comparative and functional genomics, and microbial diversity. E-mail: [email protected] Valérie Reeb Debashish Bhattacharya 409 J. Seckbach and D.J. Chapman (eds.), Red Algae in the Genomic Age, Cellular Origin, Life in Extreme Habitats and Astrobiology 13, 409–426 DOI 10.1007/978-90-481-3795-4_22, © Springer Science+Business Media B.V. 2010 THE THERMO-ACIDOPHILIC CYANIDIOPHYCEAE (CYANIDIALES) VALÉRIE REEB1 AND Debashish Bhattacharya2 1Department of Biological Sciences and the Roy J. Carver Center for Comparative Genomics, University of Iowa, Iowa City, Iowa 52242, USA 2Department of Ecology, Evolution and Natural Resources, Rutgers University, NJ 08901, USA 1. Introduction 1.1. BACKGROUND Extremophiles are organisms that thrive in environments previously thought inhospitable to life because the physicochemical characteristics fall outside the range tolerated by human cells. These types of environments are usually fatal to most eukaryotes, but have been shown to host a diverse group of prokaryotes that rely on specialized enzymes for survival. Extremophiles are permanently exposed to harsh environmental conditions and are categorized according to their ability to thrive in a specific type of niche. For example, thermophiles grow at tempera- tures above 50°C, psycrophiles prefer temperatures below 15°C, piezophiles are pressure-lovers, halophiles are found in high salt concentrations, whereas acido- philes and alkaliphiles thrive at an extreme pH of £ 3 and ³ 10, respectively. These taxa are found in hot and cold deserts, hot springs, salt lakes, in sulfide mines, or near deep-sea vents all around the world. It has been speculated that if extrater- restrial life exists, it would be in the form of an extremophile. The unicellular red algae Cyanidiales are one of the few eukaryotes that can thrive in an extreme environment. They are defined as thermo-acidophiles because they have the remarkable ability to grow in volcanic and thermal areas under extremely low pH (0.05–5) and relatively high temperature (35–56°C). Cyanidiales are the only photosynthetic eukaryotes living under such hostile conditions. 1.2. HISTORY OF CYANIDIALES Known since the second half of the nineteenth century, these unique algae were first considered a single species and described as Coccochloris orsiniana by Meneghini (1839). However, due to their simple morphology and lack of diagnostic features, this alga was assigned many different names and classified in various algal divisions (Chlorophyta, Cryptophyceae, Cyanophyta, Rhodophyta) in the 411 412 VALÉRIE REEB AND Debashish Bhattacharya ensuing years (see Ott and Seckbach, 1994 for a review). It was not until 1933 that Geitler gave it the generally accepted binomial Cyanidium caldarium and the taxon was officially recognized as part of the Rhodophyta by Hirose (1958), who demonstrated the presence of several characteristic rhodophycean features. It was discovered only fairly recently that several species of thermo-acido- philic algae actually coexist in the same habitats (De Luca and Taddei, 1970), explaining the persisting confusion about the taxonomy of the Cyanidiophyceae. Thereafter, De Luca et al. (1978) introduced the new species Cyanidioschyzon merolae, easily recognized by its characteristic size and shape, whereas Merola et al. (1981) differentiated Galdieria sulphuraria from Cyanidium caldarium based on its ability to grow heterotrophically. In 1991, Sentsova isolated three new spe- cies of Galdieria from far eastern Russia: G. daedala, G. maxima, and G. partita that are differentiated by cell size, number of autospores produced, and plastid shape (Gross, 1999; Sentsova, 1994). Finally in 2007, Pinto et al., described a new “phylospecies” G. phlegrea that mainly differed from other Galdieria by virtue of the relative number of substitutions in the plastid-encoded rbcL gene. This spe- cies is found exclusively in endolithic sites in thermal areas in Italy. Until now, the Cyanidiales includes seven species. However, with the advance of molecular sys- tematics, and the exploration of new environments, the number of recognized species of Cyanidiales is very likely to increase, perhaps dramatically. 2. Characterization of the Cyanidiales 2.1. ECOLOGY Cyanidiales are widely distributed and, according to Brock (1978), could virtually be found in every acidic hot spring around the world as long as all ecophysiologi- cal conditions are met (Fig. 1). With the increased interest in these unique algae, many volcanic regions have been explored (Negoro, 1944; Pinto and Taddei, 1978; Geitler and Ruttner, 1936; Schwabe, 1936; Brock, 1978; Sentsova, 1991; Gross et al., 1998, 2001; Ciniglia et al., 2004) and they have been recorded from all conti- nents with the exception of Africa and Antarctica (perhaps due to limited effort). Cyanidiales have been found to thrive not only in acidic hot pools and springs (Fig. 1a) but also on rocks and muddy soil around hot pools and along streams (Fig. 1c) and in fissures in rock walls (interlithic) or under a thin layer of rock (endolithic) that is exposed to acidic sulfur fumes (Fig. 1b). Cyanidiales grow optimally at 45°C but can be found in environments with a temperature up to 55–56°C. The lower limit in aquatic habitats is around 35–36°C because below these temperatures, there is apparently too much compe- tition with other acidophilic algae for their persistence. In contrast, they can be found in soil with temperatures as low as 10°C where competition is apparently less marked (Doemel and Brock, 1971). The pH range at which Cyanidiales grow is between 0.05 and 5, with the optimum at pH 2–3 (Doemel and Brock, 1971). THE THERMO-ACIDOPHILIC CYANIDIOPHYCEAE (CYANIDIALES) 413 Figure 1. Images of Cyanidiales in their natural environment. (a) Cyanidiales growing as a thick mat in the runoff from an acidic hot spring. (b) Endolithic Cyanidiales growing under a crust of rock deposits. (c) Cyanidiales growing on a rock surface that is exposed to sulfur fumes. All of these sites are found at Yellowstone National Park in the USA. Members of the Cyanidiophyceae have also been rarely found in nonther- mal and nonacidic habitats. Schwabe (1936) was the first to record Cyanidium from caves along the coast of central and southern Chile. Additional “cave” Cyanidiales were recorded from France (Leclerc et al., 1983), Israel (Friedmann, 1964), and Italy (Skuja, 1970; Ciniglia et al., 2004). Caves have a specific micro- climate: stable, low temperatures (4–10°C), slightly acidic to alkaline (pH 5–7), constant and high level of humidity, and low light intensity. Although these ecological features are radically different from those associated with the “typical” Cyanidiales, Cyanidium from caves have morphological characteristics that are virtually indistinguishable from their thermo-acidophilic counterparts (Hoffman, 1994). In fact cave taxa show a close phylogenetic relationship to Cyanidium caldarium based on molecular data (Ciniglia et al., 2004). During their survey of 120 acidic sites in Italy, Pinto and Taddei (1978) documented the presence of C. caldarium not only from hot springs, but also nonthermal sites such as sulfur mines where sulfidic ores lead to the establishment of low pH conditions. Galdieria strains were recorded together with chlorophytes and Cyanobacteria from a sulfur mine, a peat bog, and diatomite shield exposed to oxygen at Soos in Czech Republic (Gross et al., 2002). Finally, Cyanidiales have been reported in freshwater contaminated by acid mine drainage (AMD) that displays extremely low pH and high metal concentrations (Moreira et al., 1994; Gross, and Gross, 2001; Aguilera et al., 2007; Baker et al., 2004). The extremely low pH of these waters is due to the dissolution and oxidation of sulfidic minerals (sulfides) in rock strata that are exposed to water and oxygen (Novis and Harding, 2007). In turn, the low pH facilitates metal solubility in water, and therefore AMD waters tend 414 VALÉRIE REEB AND Debashish Bhattacharya to have high concentrations of heavy metals (Johnson, 1998). It is possible that a greater diversity of red algae may be present in mine environments than has been identified thus far. For instance, Moreira et al. (1994) reported at least three strains of Galdieria from the Rio Tinto (Spain). Currently, there are no available nucleotide sequences of Cyanidiales from mines and their phylogenetic placement is still unknown. Therefore, these intriguing environments deserve more attention in the future. Until now, there have been no reports of Cyanidiales from basic freshwater or seawater habitats (Brock, 1978; Gross, 1999). Cyanidiales also have the ability to grow under low light conditions, for instance in endolithic conditions where the algae that are covered by a silica sinter receive less than 1% of daylight for photosynthesis, or within caves up to 40 m from the entrance where direct light reaches the algal colonies only rarely (Gross et al., 1998; Leclerc et al., 1983). Growth in crypto-endolithic habitats or caves is most likely a strategy to avoid desiccation, but requires special adaptations for the organism to survive under reduced light intensity. Autotrophic growth at endo- lithic sites is possible only within the first few millimeters beneath the surface layer (Gross and Oesterhelt, 1999).
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