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Cyanobacteria in Hypersaline Environments: Biodiversity and Physiological Properties

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Cyanobacteria in Hypersaline Environments: Biodiversity and Physiological Properties Biodivers Conserv (2015) 24:781–798 DOI 10.1007/s10531-015-0882-z REVIEW PAPER Cyanobacteria in hypersaline environments: biodiversity and physiological properties Aharon Oren Received: 7 July 2014 / Revised: 3 February 2015 / Accepted: 12 February 2015 / Published online: 3 March 2015 Ó Springer Science+Business Media Dordrecht 2015 Abstract Within the cyanobacterial world there are many species adapted to life in hypersaline environments. Some can even grow at salt concentrations approaching NaCl saturation. Halophilic cyanobacteria often form dense mats in salt lakes, and on the bottom of solar saltern ponds, hypersaline lagoons, and saline sulfur springs, and they may be found in evaporite crusts of gypsum and halite. A wide range of species were reported to live at high salinities. These include unicellular types (Aphanothece halophytica and similar morphotypes described as Euhalothece and Halothece), as well as non-hetero- cystous filamentous species (Coleofasciculus chthonoplastes, species of Phormidium, Halospirulina tapeticola, Halomicronema excentricum, and others). Cyanobacterial di- versity in high-salt environments has been explored using both classic, morphology-based taxonomy and molecular, small subunit rRNA sequence-based techniques. This paper reviews the diversity of the cyanobacterial communities in hypersaline environments worldwide, as well as the physiological adaptations that enable these cyanobacteria to grow at high salt concentrations. To withstand the high osmotic pressure of their surrounding medium, halophilic cyanobacteria accumulate organic solutes: glycine betaine is the pre- ferred solute in the most salt-tolerant types; Coleofasciculus produces the heteroside glucosylglycerol, and the less salt-tolerant cyanobacteria generally accumulate the disac- charides sucrose and trehalose under salt stress. Some cyanobacteria growing in benthic mats in hypersaline environments are adapted to life under anoxic conditions and they can use sulfide as an alternative electron donor in an anoxygenic type of photosynthesis through a process which involves photosystem I only. Keywords Cyanobacteria Á Hypersaline salterns Á Osmotic adaptation Á Anoxygenic photosynthesis Communicated by Anurag Chaurasia. A. Oren (&) Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904 Jerusalem, Israel e-mail: [email protected] 123 782 Biodivers Conserv (2015) 24:781–798 Introduction Cyanobacteria are the main primary producers in inland hypersaline lakes, coastal hypersaline lagoons, saltern evaporation ponds for the production of salt from seawater, saline springs, and other environments with salt concentrations exceeding that of seawater (3.5 %). In contrast to most groups of eukaryotic micro- and macroalgae, the cyanobacteria contain many members adapted to life at elevated salt concentrations. Green algae, diatoms, dinoflagellates and other eukaryotic phototrophic microorganisms generally perform very poorly at salt concentrations above 10 %. But in shallow hypersaline lakes, in saltern evaporation ponds, and in other light- exposed environments with high salt concentrations cyanobacteria often form dense benthic mats with high photosynthetic activities (Caumette et al. 1994;Cohen1984; Corne´eetal. 1992; Des Marais 1995, Ionescu et al. 2007;Krumbeinetal.1977;Orenetal.1995;Rˇ eha´kova´ et al. 2009; Schneider et al. 2013). Both unicellular and filamentous types participate in the formation of these mats. Although generally less conspicuous than the benthic mat-forming relatives, planktonic halophilic cyanobacteria also exist. At the highest salt concentrations—from about 25 % up to NaCl saturation— cyanobacteria are rarely found, and primary production is mainly due to activity of eukaryotic green algae of the genus Dunaliella. However, there are exceptions. For ex- ample, halite evaporites in the Atacama Desert, Chile, contain viable and active unicellular cyanobacteria morphologically resembling Chroococcidiopsis (Wierzchos et al. 2006) but phylogenetically closer to Halothece (de los Rios et al. 2010). There are more such reports of the occurrence of cyanobacteria in evaporite crusts (Rothschild et al. 1994). The first treatise on cyanobacteria living in hypersaline environments is probably the 1933 paper by Hof and Fre´my titled ‘‘On Myxophyceae living in strong brines’’. In this paper the authors described Aphanothece halophytica as a new species of unicellular cyanobacteria. Aphanothece and similar forms described as Halothece and Euhalothece spp. are among the most prominent inhabitants of hypersaline environments, planktonic as well as benthic (Garcia-Pichel et al. 1998). Another key paper on cyanobacterial life at high salt concentrations is that by Golubic (1980). Realizing that cyanobacteria live over a wide range of salt concentrations and that many species can adapt to changing salinity, Golubic divided the organisms into euryhaline species that live in a wide salinity range and stenohaline types whose distribution is restricted to a narrow range of salt concentrations. He further classified the species as oligohaline, mesohaline, and polyhaline, for types growing optimally at low, intermediate and high salt concentrations, without proposing the boundaries separating these categories. Indeed, it is not feasible to divide the cyanobacteria into well-defined groups based on their salt tolerance and salt requirement. This paper reviews the biodiversity and the physiology of halophilic/halotolerant cyanobacteria, a group operationally defined here as requiring (halophilic) or tolerating (halotolerant) salt concentrations above *5 %, i.e. one and a half times that of seawater. The biology of cyanobacteria living in high-salt environments has been reviewed several times in the past, most recently in a comprehensive review by Oren (2012). Therefore special emphasis in this short review will be on the most recent advances in the field. Diversity of cyanobacteria in hypersaline environments as assessed by microscopy and culture-dependent approaches Many surveys have been published of the cyanobacterial diversity in hypersaline envi- ronments. In older studies, as well as in many newer ones, identification of the taxa is 123 Biodivers Conserv (2015) 24:781–798 783 based on morphological characters. In recent years, molecular characterization based on 16S rRNA gene sequencing became increasingly used for the taxonomic characterization of cyanobacteria, in cultures as well as in natural samples. A recurrent problem when comparing data from different studies is the confusing state of the cyanobacterial nomenclature and taxonomy. Different classification systems have been devised over the years, and organisms are often known under more than one name. The situation is further complicated by the fact that the nomenclature is covered by two Codes of Nomenclature: the International Code of Nomenclature for algae, fungi, and plants (the ‘Botanical Code’) and the International Code of Nomenclature of Prokaryotes (the ‘Bacteriological Code’). Only very few cyanobacteria genera and species were named under the provisions of the International Code of Nomenclature of Prokaryotes, including one halophilic representative: Halospirulina tapeticola (Nu¨bel et al. 2000b). In most cases the names listed in this paper are those used in the original publications. An exception is made for Microcoleus chthonoplastes, which was renamed C. chthonoplastes based on morphological and molecular studies of Microcoleus species from salty and from fresh- water environments (Siegesmund et al. 2008). Table 1 summarizes the distribution of different types of cyanobacteria (morphological identification to the genus level) in a number of hypersaline environments and other high-salt habitats of special interest in which cyanobacteria are an important part of the biota: Great Salt Lake (Utah), saltern evaporation ponds, the lagoons of Guerrero Negro (Baja California) Solar Lake (Sinai, Egypt), Hot Lake (Washington), hypersaline lagoonal mats on San Salvador Island (Bahamas), the stromatolites of Shark Bay (Western Aus- tralia), and the Great Salt Plains (Oklahoma). When dividing the environments according to the salinity range (5–15, 15–22 and [22 % total dissolved salts), it is obvious that the higher the salt concentration, the smaller the diversity of cyanobacteria encountered. At the highest salinities filamentous cyanobacteria such as Coleofasciculus, Phormidium and Halospirulina that dominate in the intermediate salt concentration range are rarely seen. The only form adapted to life at salt concentrations approaching NaCl saturation is the unicellular type represented by the Aphanothece–Halothece–Euhalothece cluster. The environments studies and listed in Table 1 include: – Great Salt Lake, Utah, which is divided by a causeway into the less saline south arm (salinity *6–10 %) and the northern part which is currently approaching NaCl saturation. A. halophytica is a characteristic inhabitant of the higher-salinity sites (Brock 1976; Roney et al. 2009). The most important cyanobacterium living in the less- saline southern basin is the nitrogen-fixing heterocystous Nodularia spumigena (Roney et al. 2009). Heterocystous cyanobacteria are seldom encountered anywhere at salt concentrations exceeding 10 %. – Solar Lake (Sinai, Egypt), on the shore of the Gulf of Aqaba, Red Sea, is a small hypersaline heliothermal lake. In summer the lake
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