Cyanobacteria: From Basic Science to Applications

Brazil

Preface

A.K. Mishra

D.N. Tiwari

A.N. Rai

Cyanobacteria are a unique group of gram-negative prokaryotes having oxygenic photosynthesis and have the distinction of being the oldest known fossils, more than 3.5 billion years old. Many of them also carry out N2 fixation. They are considered as the Earth’s architect because their oxygen evolving property has led to the formation of oxygen atmosphere on this planet. They are thought to be the ancestors of plant chloroplast with the help of which plants make food for themselves. Despite being prokaryotic in nature, cyanobacteria exhibit a number of similarities with eukaryotic algae, hence are often called blue-green algae. These organisms have been tremendously important in shaping the course of evolution and ecological change throughout the Earth’s history. They occur as free-living forms as well as in a wide range of symbioses with plants ranging from algae to angiosperms. The role of N2-fixing cyanobacteria as natural biofertilizers, particularly in rice fields, as well as their application in reclamation of alkaline usar soils are well documented. Cyanobacteria are able to coordinate and synchronize different bioenergetic and metabolic processes using temporal and spatial separations as a strategy within and between their extremely small sized cells. Cyanobacteria also have been found to be an important source of various bioactive compounds having pharmacological, industrial, and biotechnological applications. Cyanobacteria are frequently used as bioremediation agents for the removal of toxic pollutants from the environment because they inhabit a number of polluted sites and exhibit increased tolerance against those toxicants.

Considering these interesting aspects of their biology and their spectacular contributions to the environment as well as human welfare, we have compiled this book which covers various important facts about cyanobacteria starting from diversity, taxonomy, and distribution to their metabolic regulation and applications. This book logically explores different topics related to cyanobacteria in well documented and profusely illustrated 24 individual chapters contributed by nationally and internationally recognized authors having excellence in teaching and research in the field of cyanobacteria and plant science. The book comprises details of cyanobacterial diversity, molecular taxonomy, the molecular basis underlying the development and function of specialized structures such as heterocytes and akinetes, biochemical and physiological background of nitrogen fixation and hydrogen production, occurrence of cyanobacteria as symbionts and their ecophysiology in extreme polar habitats. Moreover, the book is also enriched by skillful description about cyanobacterial photosynthesis, photomorphogenesis, and photoprotection mechanisms along with siderophore dependent and independent strategies of iron homeostasis. Besides, a significant portion of the book is dedicated to elucidate the cellular mechanisms of cyanobacteria to cope up with various environmental stresses (such as metal and pesticide toxicity), their plant growth promoting properties, their secretion systems, commercial importance of their exopolysaccharides and phycobiliproteins, their potential as bioenergy and biofuel resources, and their biotechnological applications. Monitoring ecotoxicity of antibiotics in fresh water using cyanobacteria and the inside story of cyanobacterial toxins are also catalogued in this book.

We hope that this edited volume will serve as a valuable resource to the undergraduate and postgraduate students as well as researchers working on cyanobacteria. Using this book, teaching institutions should find it helpful in framing up to date syllabi on cyanobacteria.

We affirm our indebtedness to all the contributors for their cooperation and valuable contributions without which this book would have not been possible. We sincerely thank Dr. P.K. Singh, FNA, Prof. S.P. Singh, Prof. B.R. Chaudhary, Dr. S.S. Singh (Banaras Hindu University), and Dr. Piyush Chaturvedi (Cambridge University) for their valuable suggestions.

We owe our deep felt gratitude and affection to our families whose blessings and supports inspired us to complete this task. We also thank Head, Department of Botany, BHU, for providing necessary facilities.

Chapter 1

Cyanobacteria in Diverse Habitats

Lira A. Gaysina⁎,†; Aniket Saraf‡; Prashant Singh§    ⁎ Department of Bioecology and Biological Education, M. Akmullah Bashkir State Pedagogical University, Ufa, Russian Federation

† All-Russian Research Institute of Phytopathology, Moscow, Russian Federation

‡ Department of Botany, Ramniranjan Jhunjhunwala College, Mumbai, India

§ Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, India

Abstract

Cyanobacteria are an enormously diverse group of prokaryotes whose adaptive capacity along with the ability to tolerate extreme conditions makes them omnipresent. They are found in almost all the habitats of the Earth where life can be imagined to have flourished. Cyanobacteria are present in a wide range of habitats viz. marine, freshwater, soil, biological soil crusts, snow, cryoconites, etc. Further, they are found in symbiotic association with different hosts and also occur in extreme stressed conditions like volcanic ash, salted soils, and anthropogenically disturbed areas. This chapter explores the diversity of cyanobacteria from different habitats and enlists the dominant groups inhabiting these habitats. The diversity of cyanobacteria from different climatic zones; temperate, tropical as well as Polar Regions have been reviewed and documented in this chapter. The taxonomic complexity of cyanobacteria has hindered the capture of the actual biodiversity which is evident from the fact that the reported diversity encompasses only the traditional cyanobacterial genera. Morphological plasticity, ecological flexibility, and huge amount of heterogeneity are responsible for the confusions surfacing the cyanobacterial taxonomy. In this chapter, we also discuss the current trends in cyanobacterial taxonomy which would be essential in the studies conducted to capture the biodiversity of cyanobacteria from different habitats.

Keywords

Cyanobacteria; Biodiversity; Plankton; Benthos; Biological soil crusts; Volcanic ash; Disturbed areas; Salted soils; Polar Regions; Polyphasic approach; Prochlorococcus; Synechococcus; Nodularia; Nostoc; Microcoleus vaginatus

Acknowledgments

This work was supported by the Russian Foundation for Basic Research in the frame of project 16-04-01511 а. PS and AS thank the Department of Science and Technology (DST-SERB) for the project PS/YSS/000879. The authors are thankful to Jeffry R. Johansen for valuable discussion, and Yunir Gabidullin for helping us in the preparation of the figure plates.

1 Introduction

Cyanobacteria are oxygen evolving, gram-negative, photoautotrophic bacteria that can be found in virtually all imaginable habitats across the world. They can be found in habitats extending from the extremely cold deserts of the Arctic and Antarctic Zones (Mataloni and Komárek, 2004) to the very extreme hot springs of the Yellowstone National Park, thus representing an interesting form of life in a wide range of aquatic and terrestrial environments (Whitton and Potts, 2000a,b). This extraordinary expanse of cyanobacteria is actually a result of an important character that the cyanobacteria can boast of which we refer to as adaptability. Their amazing success in adapting to such diverse and varying habitats can be attributed to a very long-standing evolutionary history that cyanobacteria enjoy. Some of the modern physiological and anatomical features of cyanobacteria that have helped in supporting their long history on Earth include an extremely high tolerance level of low oxygen and free sulfide, the ability to utilize H2S as a photoreductant in place of H2O, and the strong tolerance capacity for ultraviolet B and C radiations (Whitton and Potts, 2000a,b). Thus, these are some of the major adaptive features that have allowed the cyanobacteria to grow, flourish, and dominate in habitats where many other forms of life are absolutely unknown or may struggle to even survive.

Interestingly, the origin of cyanobacteria and their basic anatomical features are typical bacterial type but their ecological, biological, and morphological features are quiet specific and diverse too (Flores et al., 2006; Kalaitzis et al., 2009; Flores and Herrero, 2010). The almost essential possession of some interesting features like the ability of buoyancy, performing oxygenic photosynthesis, and fixation of atmospheric nitrogen (Walsby, 1994; Castenholz, 2001; Burja et al., 2001; Berman-Frank et al., 2003) make the cyanobacteria more special and capable to adapt to varied conditions in both normal and stressed habitats. As a consequence of such strong survival capabilities, they also act as prominent phototrophic primary producers in natural ecosystems (Field et al., 1998; Bryant, 2003).

Cyanobacteria have played a major role in the evolution of different forms of life on Earth. The anaerobic earth was converted to the aerobic one by the cyanobacteria about 2 billion years ago, thus finally supplying oxygen to the atmosphere through oxygenic photosynthesis for approximately 1.5 billion years (Berman-Frank et al., 2003; Schopf et al., 1983). This event of oxygenation of the Earth’s atmosphere allowed for an enormous degree of greater diversification of many forms of life on the Earth. Apart from the oxygenation, cyanobacteria also influenced the advancement of life on Earth by shaping up themselves as the progenitors of chloroplasts (Giovannoni et al., 1988; Sergeev et al., 2002), ultimately leading to a broader diversification of algae and land plants.

In the current times, the cyanobacteria still continue to affect the life on Earth, as the major oxygen producers on this planet. Apart from being the major oxygen producers, many of them are also efficient fixers of atmospheric nitrogen thus making them extremely important components of nutrient-deprived ecosystems and extreme environments all throughout the Earth. As a result of their high adaptive capacity, cyanobacteria are also well known to form a wide range of nitrogen-fixing symbiotic relationships with representatives from almost all plant groups such as algae (Hemiaulus hauckii-Richelia intracellularis) fungi (Geosiphon pyriforme-Nostoc), bryophytes (Anthoceros-Nostoc), pteridophytes (Azolla-Anabaena), gymnosperms (Cycas-Nostoc), and angiosperms (Gunnera-Nostoc), thus supplying the host organisms with a lot of fixed nitrogen and in return, acquiring carbohydrates from the host (Morot-Gaudry and Touraine, 2001), thus allowing the host organisms to grow in regions where they may otherwise not survive at all.

Cyanobacterial diversity owing to their adaptive capacities occupies incredibly large canvas of the planet Earth. The expanse of their diversification spreads in almost all the habitable ecosystems on the Earth. Along with having an omnipresent occurrence with large ecological benefits, cyanobacteria are also one of the most important contributors to the global nitrogen fixation and carbon fixation chains (Karl et al., 2002). Their physiological plasticity and level of flexibility are of scales that are enormous in magnitude, thus enabling them to be active representatives of virtually all geographical sections on the planet Earth (Kol, 1968; Castenholz, 1973; Whitton, 1973; Van Landingham, 1982; Reed et al., 1984; Kann, 1988; Dor and Danin, 1996; Laamanen, 1996; Skulberg, 1994; Weber et al., 1996). Many of them are luxuriantly growing freshwater forms, but many of the cyanobacterial taxa thrive equally well in marine environments. Terrestrial habitat and biological crusts are indeed common for the majority of the strains of the cyanobacteria along with a strong presence in the benthic habitats. Due to their extraordinary physiologically adaptive capacity, cyanobacteria are also equally proficient in forming frequent and useful endophytic and symbiotic associations (Rai, 1990; Adams, 2000; Bergman et al., 2007; Thajuddin et al., 2010). They are known to form biofilms and microbial mats on shores, surface of the stones, plants, and artificial objects especially in extreme habitats (Stal, 2000). The frequent and heavy occurrence of cyanobacteria in freshwater bodies (Fig. 1A–C), seepages, rocky crevices, the bark of trees, rice fields, within limestone, salt subjugated lands, marine ecosystems, deserts, polar environments (Fig. 1D–F), biological soil crusts (BSCs) (Fig. 1H and I), soil surface (Fig. 1J), and in symbiotic associations, thus emphasizing their ability to survive and flourish in the above niches with ease and competence (Whitton and Potts, 2000a,b; Elster et al., 1999).

Fig. 1 Cyanobacteria in diverse habitats: (A) freshwater dwelling cyanobacteria in small rivulets, India; (B) freshwater dwelling cyanobacteria in shallow water bodies, India; (C) cyanobacteria in stagnant freshwater bodies, India; (D) freshwater dwelling cyanobacteria in shallow Arctic water body; (E) freshwater dwelling cyanobacteria attached on stones in shallow Arctic water body; (F) almost dried cyanobacterial mat on decomposed soil in the Arctic; (G) cyanobacteria-dominated pediceled algal crust in Grand Staircase-Escalante National Monument, Utah, United States; (H) cyanobacterial crust in South Ural region, Russia; (I) polygonal lichen-dominated crust in steppe in South Ural region, Russia; (J) visible growth of algae and cyanobacteria on wet soil in South Ural region, Russia.

However, in spite of their importance in many ecosystems, cyanobacteria have been neglected in many biodiversity studies (Rejmánková et al., 2004). The hidden biodiversity of cyanobacteria is very high, especially in understudied and less explored geographic regions (Nabout et al., 2013; Gaysina et al., 2018). As morphological features have traditionally been the main criterion for classifying and identifying cyanobacteria, most of the studies carried out to date relied almost exclusively on less discriminative morphology-based methods (Alvarenga et al., 2015).

2 Cyanobacteria in Aquatic Habitats

2.1 Marine Cyanobacteria

Oceans and seas are the largest ecosystems on the planet. The oceans cover 71% of the Earth’s surface, with 50% of the depth being below 3000 m and a mean depth of about 3800 m (Ramirez-Llodra et al., 2010). Cyanobacteria inhabit a wide range of niches in marine ecosystems, where they occupy maritime coasts and the open ocean. Aquatic cyanobacteria are divided into two large ecological groups: planktonic cyanobacteria that float freely in the water column and benthic cyanobacteria that adhere to submerged solid surfaces (sediments, rocks, stones, algae, and aquatic plants) (Fogg et al., 1973). The ecological conditions in these two habitats are different and that is why the biodiversity of the benthic and planktonic species should be considered separately (Hoffmann, 1999).

2.1.1 Marine Plankton

Planktic cyanobacteria are adapted to vertical migrations using the phenomena of buoyancy regulation. Another adaptive mechanism is the production of aerotopes, containing gas vesicles (Reynolds et al., 1987; Brookes and Ganf, 2001).

The marine cyanobacteria Prochlorococcus and Synechococcus are dominant in many ocean regions (Flombaum et al., 2013). The cyanobacterial genus Prochlorococcus was isolated about 20 years ago. Probably, it is the most abundant photosynthetic organism on the planet (Scanlan et al., 2009). Prochlorococcus is dominant in phytoplankton communities in the central oceanic parts up to a depth of about 150 m 40°N and 40°S. It has been hypothesized that its population size is limited by latitudes, and hence Prochlorococcus is understandably absent at temperatures below 15°C (Moore et al., 1995; Partensky et al., 1999; Zubkov et al., 2003; Johnson et al., 2006). This taxon also exhibits significant genetic diversity, which has resulted in differences in light and temperature sensitivities and nitrogen adaption abilities (Johnson et al., 2006; Moore et al., 2002, 2008; Moore and Chisholm, 1999; Rocap et al., 2003).

Synechococcus distribution is not as deep as Prochlorococcus, but it has a wider geographical distribution in both polar and high-nutrient waters (Zubkov et al., 2003; Moore et al., 1995; Partensky et al., 1999). The genera Cyanobium and Synechocystis are also widely distributed in marine planktonic communities (Costa et al., 2014). Some species of the filamentous genus Romeria have also been found in marine planktons (Komárek, 2001).

In favorable conditions, cyanobacteria grow rapidly and form blooms (Sellner, 1997; De Figueiredo et al., 2006; Sciuto and Moro, 2015). They exist in highly productive nutrient-rich waters by having gas vesicles supporting the migration between the surface and bottom waters (Paerl et al., 2001).

Trichodesmium is an example of a colonial filamentous cyanobacteria. It is one of the most abundant bloom-forming species in the marine pelagic zone, characterized by a panglobal distribution in oligotrophic environments in tropical and subtropical oceans (Capone et al., 1997; LaRoche and Breitbarth, 2005). Trichodesmium has the ability to even grow above 20°C and thus may expand its distribution in the conditions of global warming (Hutchins et al., 2007; Stal and Zehr, 2008).

The nitrogen-fixing coccoid genus Crocosphaera has also been detected in tropical waters (Zehr et al., 2007). Crocosphaera watsonii is well known as a significant contributor to oceanic nitrogen fixation (Zehr et al., 2001; Montoya et al., 2004; Moisander et al., 2010). Crocosphaera is also able to reduce its iron-metalloenzyme inventory. It allows Crocosphaera to inhabit regions low in iron (Saito et al., 2011).

In estuarine environments cyanobacterial blooms have been detected in all basins of the central Baltic Sea (Karjalainen et al., 2007). Intensive growth of blooms has been reported in many areas, where these communities were rare before (Kahru et al., 1994; Mazur-Marzec et al., 2006).

The genera Nodularia, Aphanizomenon, and Anabaena belong to the most important bloom-forming cyanobacteria in the Baltic Sea (O’Neil et al., 2012). In this ecosystem, cyanobacteria Nodularia spumigena forms toxic blooms each summer (Teikari et al., 2018). It is necessary to note that among Nodularia both planktonic and benthic species exist: Nodularia baltica, N. litorea, and N. spumigena are planktonic species, while N. harveyana and N. spaerocapsa are benthic species (Komárek et al., 1993).

2.1.2 Marine Benthos

Benthic filamentous cyanobacteria usually possess unique gliding motility (Hoiczyk, 2000). This group of cyanobacteria can form mats—dense multilayered communities of many species, which grow on sediments of different environments (Stal, 1995).

Filamentous cyanobacteria of the genus Lyngbya can be found in benthic communities worldwide, where it forms dominant cover and blooms in tropical and subtropical coral reef and seagrass habitats (Paul et al., 2005; Jones et al., 2011; O’Neil et al., 2012). Lyngbya is an important contributor to coral reef ecosystems, occasionally forming the dominant cover and impacting the health of many other co-occurring organisms. Lyngbya majuscule belongs to the benthic cyanobacteria and is widely distributed in tropics in reef and lagoons, forming dense mats (Hoffmann, 1994; Whitton and Potts, 1982, 2000a,b; Thacker and Paul, 2004). In Guam and the Republic of Palau, several Lyngbya species, including Lyngbya majuscule, have been detected (Thacker and Paul, 2004). During the study of benthic bloom forming Lyngbya in Broward County, Florida using polyphasic approach, it was found that this bloom contains a new species of Lyngbya. The second most common Lyngbya in this habitat was similar to Lyngbya polychroa (Paul et al., 2005). The filamentous cyanobacterial genus Moorea belongs to a cosmopolitan pantropical ecological group, abundant in the marine benthos. Members of this genus are photosynthetic, nondiazotrophic, and often create mats or blooms in shallow water (Engene et al., 2012). The genera Coleofasciculus, Hydrocoleum, and Lyngbya are dominant in all the sediment types in cyanobacterial populations in intertidal flats of the German Wadden Sea (Vogt et al., 2018). Cyanobacteria Microcoleus ethnoplasts and representatives of the genera Spirulina and Oscillatoria sp. belong to common species in marine intertidal and littoral habitats (Kulasooriya, 2011). The filamentous genus Nodosilinea, Leptolyngbya, Pseudanabaena, and Romeria constitute a large group of the marine cyanobacterial strains, usually isolated from the Portugal coast (Costa et al., 2014). In all, 26 species of cyanobacteria were included in the checklist of benthic marine algae and cyanobacteria of Northern Portugal with 15 species belonging to the order Oscillatoriales (Sousa-Pinto, 2009). Lyngbya was the richest in species genus (Araujo et al., 2009).

Recent studies based on phylogenetic inference of small-subunit (SSU) rRNA genes have revealed a large extent of novel biodiversity of benthic cyanobacteria from tropical and subtropical marine environments (Engene et al., 2013). Among the 10 phylogenetic clades of natural product-producing strains from benthic environments, only two clades were related to reference or type strains of cyanobacteria. Thus, the biodiversity in tropical marine forms of cyanobacteria are unclear and definitely need further investigations.

2.1.3 Mangroves

Mangrove forest is an example of transitional ecosystems between the coast and the mainland (Rigonato et al., 2013). A number of surveys of the cyanobacterial diversity of mangroves of several tropical and subtropical regions of the world have been published (Branco et al., 1996, 1997; Silambarasan et al., 2012; Silva et al., 2014; Alvarenga et al., 2015). Genera Aphanocapsa, Calothrix, Chroococcus, Coleofasciculus, Lyngbya, Oscillatoria, and Schizothrix comprise the most widespread cyanobacterial mangrove dwellers across the world (Alvarenga et al., 2015).

It is necessary to note that using culture-independent approaches the estimates of the hidden biodiversity of cyanobacteria can be evaluated up to a certain extent. Interesting data was published about the biodiversity of cyanobacteria of mangrove soils in Southeast Brazil (Rigonato et al., 2013). Molecular-genetic analysis of 16S rRNA gene sequences showed high cyanobacterial diversity. In all, 15 different cyanobacteria genera were detected in the mangrove soils, represented by sequences of the genera Aphanocapsa, Cyanobium, Cyanothece, Gloeothece, Synechococcus, Prochlorococcus, Leptolyngbya, Nostoc/Anabaena, Arthronema, Limnothrix, Oscillatoria, Phormidium, Tolypothrix, Tychonema, and Xenococcus. In addition, sequences matching uncultured cyanobacterial 16S rRNA genes were abundant in all sites sampled, indicating the existence of many potentially novel cyanobacteria. On sites close to seashore, mainly the genera Prochlorococcus and Synechococcus were found while other mangrove niches were mostly inhabited by uncultured cyanobacteria.

2.2 Freshwater Cyanobacteria

Cyanobacteria are known to flourish in freshwater habitats. They also inhabit in water bodies that maybe salty, brackish, or fresh, in cold and hot springs, and in environments where almost no other microalgae can even exist (Mur et al., 1999).

There are several classifications of ecological groups of freshwater cyanobacteria. Mur et al. (1999) described several ecostrategies of survival of freshwater cyanobacteria: scum-forming ecostrategists, stratifying ecostrategists, nitrogen-fixing cyanobacteria, and small colonial and benthic cyanobacteria. We think that scum-forming ecostrategists, stratifying ecostrategists, and small colonial cyanobacteria belong to the planktonic species, nitrogen-fixing cyanobacteria includes both planktonic and benthic representatives. Below, we will focus on the biodiversity of these ecological groups.

2.2.1 Freshwater Plankton

The autotrophic picoplanktons represent the major primary producers in the ocean and large transparent lakes (Callieri and Stockner, 2002; Ting et al., 2002). Single cells and microcolonies of picocyanobacteria (Pcy) are widely distributed in lakes around the world. The single-celled Pcy populations are predominant in large, deep oligo-mesotrophic lakes while the microcolonies prefer warmer, shallower, and more nutrient-rich lakes (Callieri, 2010). Picoplanktons consist predominantly of cyanobacteria < 3 μm in size (Ivanikova et al., 2007). Representatives of these ecological groups very rarely create stable scums through buoyancy regulation (Mur et al., 1999).

Autotrophic picoplanktons in oligotrophic lakes are dominated by the phycoerythrin-rich freshwater Synechococcus (Fig. 2A) (Fahnenstiel and Carrick, 1992; Ting et al., 2002). Analysis of 16S ribosomal DNA of freshwater Synechococcus species revealed that it is a polyphyletic genus (Urbach et al., 1998; Robertson et al., 2001). In freshwater ecosystems, the genera Cyanobium and Synechocystis are also very important (Stockner, 1988; Albertano et al., 1997; Komárek, 2003). The genus Aphanothece (Fig. 2B) forms large populations in freshwater bodies (Mur et al., 1999). The cyanobacterial genera Chroococcus, Cyanodictyon, Rhabdoderma, Merismopedia (Fig. 2C), Coelosphaerium, Coelomoron, Snowella, and Gomphosphaeria are also common in freshwater ecosystems (Komárek and Anagnostidis, 1999; Komárek, 2003).

Fig. 2 Freshwater and terrestrial cyanobacteria: (A) Synechococcus aeruginosus ; (B) Aphanothece stagnina ; (C) Merismopedia tenuissima ; (D) Lyngbya sp.; (E) Nostoc punensis ; (F) Hormoscilla pringsheimii ; (G) Phormidium uncinatum ; (H) cf. Trichocoleus hospitus ; (I) Cylindrospermum majus ; (J) Leptolyngbya voronichiniana ; (K) Leptolyngbya foveolarum ; (L) Microcoleus vaginatus ; (M) Nostoc cf. punctiforme ; (N) Phormidium breve ; (O) Phormidium dimorphum ; (P) Trichormus variabilis . Scale bars = 10 μm, for (B–L, N–P) the bar is placed in (A).

Scum-forming ecostrategists form large colonies of coccoid cells or filaments. The genera Microcystis, Anabaena, and Aphanizomenon belong to this ecological group. Microcystis is one of the most distributed taxa, which forms blooms in springs of the temperate zone and eutrophic lakes (Reynolds et al., 1981; Kurmayer et al., 2002). The high diversity and wide global distribution of common ITS gene types together with the lack of phylogeographic structure confirms the existence of intercontinental dispersal of Microcystis aeruginosa ITS types. This finding indicates that this species might be a cosmopolitan cyanobacterium (van Gremberghe et al., 2011).

Filamentous species such as Planktothrix agardhii and Limnothrix redekei belong to the homogeneously dispersed ecostrategists inhabiting eutrophic and hypertrophic shallow lakes with depth less than 3 m (Mur et al., 1999). In the eutrophic and hypertrophic shallow lakes with depth less than 3 m, the cyanobacterial diversity comprises Planktothrix agardhii and Limnothrix redekei (Mur et al., 1999). These cyanobacteria are extremely light sensitive and do not form colonies at high light intensities (Reynolds, 1997). Stratifying ecostrategists, like Planktothrix rubescens, usually dominate the intermediate zone of thermally stratified water bodies (Mur et al., 1999).

It is necessary to note that many of the cyanobacteria, including freshwater species, produce toxins (De Figueiredo et al., 2004). Microcystis belongs to the major microcystin-producer taxa in Ugandan freshwater habitats in Africa, where a significant amount of toxin has been detected in freshwater resources (Okello et al., 2010). Some species of the genera Anabaena, Planktothrix, and Nostoc can also produce microcystins (Neilan et al., 1999; De Figueiredo et al., 2004).

2.2.2 Freshwater Benthos

Benthic cyanobacteria inhabiting the bottom sediments of the water bodies usually form coherent mats (Mur et al., 1999). Benthic mats, consisting of the genera Aphanothece, Oscillatoria, and Phormidium, usually develop on the sediments of lakes and ponds. These mats later become floating mats in standing water bodies (Komárek, 2003). Leptolyngbya, Nostoc, Chroococcus, Aphanocapsa, and Aphanothece are the most distributed genera among epilithic cyanobacteria from freshwater streams of Kakoijana Reserve Forest of Assam, India (Saha et al., 2007).

Among benthic cyanobacteria, toxin-producing species also exist. In comparison with planktonic species, toxin production and species composition of toxic benthic cyanobacterial communities have been studied insufficiently (Gugger et al., 2005; Wood et al., 2007; Quiblier et al., 2013). Together with the genera Oscillatoria and Phormidium, other oscillatorian cyanobacteria Lyngbya (Fig. 2D), Leptolyngbya, Microcoleus, Tychonema, and Schizothrix are usually detected (Steppe et al., 1996; Mez et al., 1997, 1998; Hitzfeld et al., 2000; Aboal et al., 2005; Gugger et al., 2005). Together with these benthic taxa, a toxin-producing Planktothrix has been detected from a biofilm in New Zealand (Wood et al., 2010). In toxic freshwater benthic biofilms cyanobacteria, Aphanothece and Synechococcus from the order Chroococcales together with nitrogen-fixing cyanobacteria Anabaena and Scytonema from order Nostocales are usually found (Krienitz et al., 2003; Dasey et al., 2005; Mohamed et al., 2006; Mohamed, 2008; Smith et al., 2011).

Сyanobacteria using nitrogen-fixing strategy are usually dominant in deep, shallow ecosystems with low levels of inorganic dissolved nitrogen. This group includes the genera Anabaena, Aphanizomenon, Cylindrospermopsis, Nodularia, and Nostoc (Mur et al., 1999). Nostoc caeruleum, N. commune, N. microscopicum, N. parmelioides, N. pruniforme, N. verrucosum, and N. zetterstedtii forming macroscopic colonies have been reported from inland aquatic ecosystems (Mollenhauer et al., 1999). Another new species of Nostoc from freshwater habitats has been described recently from Panchvati locality of Pune, India and has been named Nostoc punensis (Fig. 2E) (Singh et al., 2015).

3 Symbiotic Cyanobacteria

Cyanobacteria are unique among the entire prokaryotes in their efficiency to form symbiotic relationships with a broad and highly varying range of hosts. This ability is partly a result of their highly efficient photosynthetic apparatus which allows them to continue this activity even at very low levels of light, which is common in the case of most of the symbiotic relationships (Usher, 2008). They play decisively the role of chloroplasts in symbioses with an array of nonphotosynthetic partners such as the marine invertebrates, where cyanobionts provide the host partners with carbon. Also, cyanobionts usually perform the process of nitrogen fixation, especially in photosynthetic partners such as diatoms, thus supplying the host with nitrogen. Interestingly, the symbiotic associations between cyanobacteria and marine organisms are one of the most important interactions in the oligotrophic waters of the global ocean, where cyanobionts make it possible for an extensive variety of marine organisms to survive in sometimes highly nutrient-deficient waters. The most common marine organisms sheltering cyanobacteria include the corals, diatoms, dinoflagellates, seagrass, and sponges.

Marine symbiotic cyanobacteria and their interactions with potential hosts, as opposed to the terrestrial symbioses, have largely remained neglected. In fact, there are just about a dozen contemporary scientific investigations of these associations and a better understanding of cyanobionts of the marine environments is indeed needed. Recent findings, anyway, open a plethora of interesting questions about the evolution of such symbiosis specificity, metabolic interactions, and cellular adaptations, all of which are areas of great interest in symbiotic research, especially because they may eventually explain the ecological impacts of cyanobionts living in the marine environment.

The symbiotic relationships are important constituents of the ecology and general life cycle pattern of many cyanobacterial lineages. These include interactions with plants (Rai et al., 2000), fungi (Rai, 1990), animals (Wilkinson, 1992), and eukaryotic algae (Janson, 2002; Murakami et al., 2004). It has been anticipated that tightly integrated ecological associations if maintained faithfully over evolutionary timescales can lead to coevolutionary patterns such as asymmetric evolutionary rates (Law and Lewis, 1983), gene-for-gene interactions (Flor, 1955), or even cospeciation (Brooks, 1979). Because the coevolution involves reciprocal evolutionary changes, it requires that each partner must have a significant fitness effect on the other (Thompson, 1994). Thus, it has been suggested that if a species somehow restricts the number of partners with which it interacts (specialization), this, in turn, may actually increase the response of that species to the selection imposed by those partners, facilitating coevolution (Whitlock, 1996; Kawecki, 1998).

It has been well recognized that the colonies of the Caribean coral Montastraea cavernosa harbor endosymbiotic cyanobacteria that express nitrogenase and, thus, fix nitrogen for the host (Lesser et al., 2007). Stable isotope results have also showed that the zooxanthellae, which have an important mutualistic symbiotic relationship with corals, actually use the products of this nitrogen fixation. As low oxygen concentrations are required to support cyanobacterial respiration and nitrogen fixation, the nitrogen fixation is confined to those times of the day when physiological hyperoxia or anoxia does not inhibit nitrogen fixation, thus maintaining an intricate balance between nitrogen fixation and photosynthesis at the same time. Through this carefully controlled process, the endosymbiotic cyanobacteria help the zooxanthellae corals to survive in oligotrophic waters by providing them with an important supplementary source of a limiting element.

Heterocytous cyanobacteria Richelia intracellularis and Calothrix rhizosoleniae are examples of some interesting taxa that live in a symbiotic relationship with many frequently occurring diatoms like Hemiaulus, Rhizosolenia, and Chaetoceros (Foster et al., 2011). These cyanobionts, in this case, are important because they provide fixed nitrogen to their nitrogen-limited hosts. This impacts both the host and the ecosystem in a positive way.

Blooms of the diatom Hemiaulus hauckii and its cyanobacterial symbiont Richelia intracellularis can reach extremely high densities and have important ecological impacts on the ecosystem. These blooms dominate the carbon deposition in the offshore tropical river plumes and thus subsidize substantially to the new N inputs (Yeung et al., 2012). The blooms of these diatom-diazotroph assemblages increase significantly the net primary productivity as well as the ecosystem carbon export ratio, which ultimately leads to the biological uptake of dissolved inorganic carbon and silicates too. Also, Hemiaulus and its nitrogen-fixing endosymbionts have been implicated as important donors to the formation of some Mediterranean sapropels (Carpenter et al., 1999). As drivers of nitrogen fixation and carbon drawdown in river plumes and oligotrophic waters, diatom-diazotroph interactions have had a global impact that is clearly an indicator of climatic and anthropogenic influences. Diatoms belonging to the family Epithemiaceae possess a unicellular nitrogen-fixing cyanobacterial endosymbiont (DeYoe et al., 1992). In case of limitations of external nitrogen, the number of endosymbionts per diatom rises, at the same time, the mean endosymbiont surface area:volume also increases. This ultimately leads to an increase in the contribution by the endosymbiont nitrogen fixation to the diatom nitrogen budget under N-limiting conditions, thus helping the diatom partner to ward of nutrient stress. This flexibility of the endosymbiont load enables the diatom to be more energy competent and contest more proficiently with other neighboring symbiotic diatoms in nitrogen-stressed habitats. Also, the diatoms that host nitrogen-fixing cyanobacterial symbionts are high in protein, which benefits the organisms that graze on these diatoms (Kupferberg, 1997). Thus, the diatom-cyanobacterial symbioses are quite widespread and also important for oceanic primary productivity.

Cyanobionts are almost omnipresent in most of the marine sponges and their microenvironments and their presence can cause noteworthy alterations in the morphology of the sponges. These cyanobacterial symbionts are generally intercellular but sometimes may occur in specialized vacuoles which are termed as cyanocytes (Usher, 2008). In this symbiosis, the photosynthates in the form of glycerol and organic phosphates are transferred from cyanobacterial partners to the sponge hosts supplying up to 50% of the sponge’s energy budget and around 80% of its carbon budget. Unicellular Synechococcus sp. is one of the most common cyanobacteria found in sponges, while nonheterocytous filamentous Oscillatoria spongeliae has also been reported over a wide geographic range (Usher, 2008). Dysidea herbacea, a commonly occurring shallow-water sponge present throughout the Indo-Pacific, harbors large numbers (up to 20% of the symbiotic association’s volume) of the cyanobacterial symbiont Oscillatoria spongeliae. By using cellular localization of some selected compounds, it has been well established that the polychlorinated metabolites attributed to Dysidea herbacea are actually localized in the symbiont Oscillatoria spongeliae. Truly, this was one of the first demonstrations that marine natural products ascribed to a sponge are actually localized in the symbiotic cells. Interestingly, these polychlorinated metabolites produced by the symbiont prevent fish feeding and thus confer augmented fitness to the sponge-cyanobacterial symbiosis (Unson and Faulkner, 1993).

Cyanobacteria-dinoflagellate symbioses are one of the foremost reasons for the widespread distribution of heterotrophic dinoflagellates in the oligotrophic subtropical and tropical oceans (Farnelid et al., 2010). Histioneis sp. and Ornithocercus sp. contain epi- or endobiotic cyanobacteria as partners. Immunolabeling-TEM using nitrogenase antisera have discovered that many cyanobionts may have a nitrogen-fixing capacity and thus probably temporally segregate their physiological processes to protect the nitrogenase enzyme (Foster et al., 2006). The mixed assemblage of a few nitrogen-fixing cyanobacteria partners residing among a larger population of nonnitrogenase localizing cyanobionts as in Histioneis depressa confers a benefit over other hosts that only contain non-N2-fixing cyanobionts partners. Thus, the dinoflagellate’s requirement for fixed nitrogen as well as carbon is the driving force for this symbiotic relationship.

The dominance of cyanobacteria in epiphytic microbial communities has been well established by using light microscopy, 16S rRNA, and nifH gene analysis methods (Hamisi et al., 2013). The nifH gene expression patterns have also demonstrated that the heterocytous phylotypes may be the dominant diazotrophs during the day while the nonheterocytous types may establish their dominance at night. Cyanobionts usually exist associated with the leaves of the seagrass Cymodocea rotundata as small attached patches of pigmented microbial aggregates of thin biofilms. Seagrass is benefitted from the diazotrophic nitrogen-fixing ability of the cyanobacteria, while the diazotrophic activity of the cyanobacteria is stimulated as indicated by the high nitrogenase levels recorded in the expression studies.

The filamentous heterocytous genus Nostoc is well known as a prolific symbiotic partner with many different eukaryotic model systems like protists, animals, fungi, and plants (Rai et al., 2002). In many phylogenetic studies, using an assortment of molecular markers (16S rRNA, rpoB, rbcLX, and nifD or nifH), the closest relatives to the genus Nostoc were shown to be the genera Anabaena, Aphanizomenon, and Trichormus, also members of the family Nostocaceae (Rajaniemi et al., 2005; Svenning et al., 2005; Henson et al., 2002, 2004; Lohtander et al., 2003; Singh et al., 2013, 2015). The genus Nostoc is characterized by a complex life cycle that includes differentiation into heterocytes (nitrogen-fixing cells), akinetes (resting spores), and hormogonia (motile filaments), which serve for dispersion and as infective units in symbiosis (Lazaroff, 1966; Lazaroff and Vishniac, 1961; Mollenhauer, 1970; Rippka et al., 1979). In some better-focussed studies, four Nostoc groups, three of which correspond to the type species Nostoc muscorum, N. edaphicum, and N. calcicola, had been resolved on the basis of their life cycle (Hrouzek et al., 2003; Rajaniemi et al., 2005), but these studies also identified many more new lineages of Nostoc morphotypes which were different to an extent, indicating that they might represent different taxa (Hrouzek et al., 2005). The symbiotic relationships of nostocacean cyanobacteria with members of the plant kingdom involve plants from various groups like Bryophyta (mosses, liverworts, and hornworts), Pteridophyta (the genus Azolla), gymnosperms (family Cycadaceae), and angiosperms (family Gunneraceae). Most of the identification and diversity studies of the cyanobionts from the individual plant hosts, with possibly the exception of Azolla, have revealed high strain diversity both within and among different host species (West and Adams, 1997; Rasmussen and Svenning, 1998; Nilsson et al., 2000; Costa et al., 2001; Guevara et al., 2002; Rasmussen and Nilsson, 2002; Zheng et al., 2002). Among the cyanobacteria associated in the symbiosis with Cycas, the species Nostoc muscorum and N. punctiforme have been identified (Costa et al., 1999). The symbiosis with the water fern Azolla is well studied, mainly due to the prospective use of Azolla as an excellent bio-fertilizer in rice fields (Van Hove and Lejeune, 2002), and also for its exceptionally continuous nature in terms of both growth and omnipresence (Lechno-Yossef and Nierzwicki-Bauer, 2002). The Azolla cyanobionts, together with few other symbionts belonging to other bacterial domain, are hosted within specialized cavities in the fronds of the fern (Lechno-Yossef and Nierzwicki-Bauer, 2002). For the first time, the cyanobionts of Azolla were described as Anabaena azollae by Strasburger (1884). However, in later years, morphological investigations of the cyanobacterial populations inhabiting the cavity, performed on the presumed cultivated cyanobionts, yielded quite confusing results on the taxonomic position of the cyanobionts (Gebhardt and Nierzwicki-Bauer, 1991). Comparative molecular studies which still are inconclusive have revealed that the cultured cyanobacteria isolated from the fern were certainly unlike the cyanobionts inhabiting the leaf cavity, leading to the equally puzzling suggestion that maybe one major cyanobacterial population is involved in the symbiosis, while other minor populations are nonspecifically associated with the fern (Tomaselli et al., 1988; Plazinski et al., 1990; Gebhardt and Nierzwicki-Bauer, 1991; Pabby et al., 2003). As of now, the taxonomy of the cyanobacterial populations living inside the fronds of Azolla remains indefinite and largely debateable. The only fact well accepted is that these cyanobionts certainly belong to the order Nostocales, with approximations of them being assigned to the genera Nostoc (Plazinski et al., 1990; Gebhardt and Nierzwicki-Bauer, 1991; Pabby et al., 2003), Anabaena (Gebhardt and Nierzwicki-Bauer, 1991; Svenning et al., 2005), Trichormus (Komárek and Anagnostidis, 1989), or all of these symbionts shifted to a new separate genus (Caudales et al., 1995; Baker et al., 2003). In an important study by Papaefthimiou et al. (2008), the phylogenetic analysis clearly showed that two distinct patterns of evolution of symbiotic behavior might be existing for the symbiotic nostocacean cyanobacteria, one leading to the symbiotic association of Nostoc species with a wide variety of plants while the other leading to the association of a unique cyanobacterial type with the water fern Azolla.

4 Terrestrial Cyanobacteria in Soil

Soil cyanobacteria belong to the well-studied group among the cyanobacteria. We should mention the reviews of F.E. Fritsch The Terrestrial Alga (1922), L.M. Shields and L.W. Durrell Algae in relation of soil fertility (1964), B. Metting The Systematics and Ecology of Soil Algae (1981), L. Hoffmann Algae of terrestrial habitats (1989), and the fundamental monograph of M.M. Gollebarch and E.A. Shtina Soil algae (1969) with special reference in this regard. Besides, the data about soil cyanobacteria have been also summarized in floristic papers (Metting, 1981).

Soil cyanobacteria are affected by a number of environmental factors: humidity, soil temperature, soil texture, рН, the concentration of salts (Gollerbach and Shtina, 1969), nutrition, and biotic interactions (Metting, 1981). Higher plants also have a significant influence on the cyanobacterial flora (Gollerbach and Shtina, 1969; Bakieva et al., 2012). We should mention that this peculiarity depends on the natural region (biome), where the cyanobacteria exist. Besides, microenvironment conditions also affect the cyanobacteria diversity. During the investigation of biodiversity of terrestrial cyanobacteria of South Ural region, humidity and heterogeneity were found to be the major factors influencing the cyanobacterial distribution. The highest cyanobacterial diversity was found in the samples from humid and/or heterogenic conditions (Gaysina et al., 2018). Therefore in the different natural regions, reside specific communities of soil cyanobacteria.

4.1 Arid Regions

Deserts and semideserts occupy extensive territories in Africa, Asia, Australia, Europe, South America, and the western parts of Northern America. Desertification is a consequence of a variety of anthropogenic activities (overgrazing by domestic livestock, harvesting of woody vegetation, soil destabilization and erosion due to off-road vehicular traffic, mining activities, global climatic change, etc.). There are numerous publications about soil cyanobacteria in arid and semiarid regions, especially about cyanobacteria in biological crusts communities. BSCs (microbiotic crusts, cryptogamic crusts) can be found in all arid regions of the world, including the Polar Regions (Büdel et al., 2009). These crusts consist of water-stable surface soil, aggregated together by algae, cyanobacteria, fungi, lichens, and mosses (Johansen, 1993). It should be noted that these BSCs play a major role in arid ecosystems, preventing soil erosion and contributing to the restoration of disturbed lands.

According to Belnap (2006), the role of cyanobacteria increases with potential evapotranspiration. In hyperarid deserts, like Atakama and Sahara, crusts are dominated by cyanobacteria, while in dryland regions, such as Northern Great Basin in United States, lichens and mosses prevail in crusts. In arid and semiarid habitats the development of cyanobacteria increases. In these conditions, crusts formation is very frequent (Gollerbach and Shtina, 1969).

During the study of biological crusts in different regions of India, genera with a distinct sheath such as Lyngbya, Plectonema, and Scytonema were dominant while the representatives of the genera Oscillatoria, Phormidium, Microcoleus, Nostoc, Calothrix, Aulosira, Fischerella, Westiellopsis, and Hapalosiphon were also very frequent (Tirkey and Adhikary, 2005). Schizothirix calcicola and Desmonostoc muscorum (formerly known as Nostoc muscorum) were found to be the dominant taxa in Baja California Desert in Mexico (Flechtner et al., 1998).

In the research of BSCs in seven major biomes in Africa along the transect from Namibian-Angolan border to the Cape Peninsula, cyanobacteria Microcoleus paludosus, Chroococcidiopsis sp., Pseudanabaena spp., Phormidium spp., Leptolyngbya spp., and Nostoc spp. were the most frequent and were detected in four biomes (Büdel et al., 2009). In a study of microbiotic soil crusts on a tiger bush sequence (Niger, Sahel) prevalence of cyanobacteria Schizothrix was detected. The genera Scytonema, Lyngbya, Microcoleus, Nostoc, and Phormidium were also very frequent (Issa et al., 1999).

A number of researchers attribute Microcoleus vaginatus to be the most widespread and ecologically important species in biological crusts around the world (Johansen and Shubert, 2001). In biological crusts in North American deserts together with the cyanobacterium Microcoleus vaginatus, Schizothrix calcicola, Nostoc commune, N. muscorum, N. paludosum, N. punctiforme, Phormidium minnesotense, Leptolyngbya tenuis (as Phormidium tenue), Trichormus variabilis (as Anabaena variabllis), and Tolypothrix tenuis have been found to be the most frequent cyanobacterial taxa (Johansen, 1993).

It is necessary to note the peculiar significance of large and mobile cyanobacteria, like Microcoleus vaginatus in crusts communities. These cyanobacteria belong to the first colonizers of bare soils. After that another species, for example, Scytonema and Nostoc, may start to grow. Mucilaginous sheaths of these species connect the soil particles and create soil aggregates (Belnap, 2006). The dominance of these taxa in arid habitats around the world is confirmed by numerous data. In desert crusts of Southeastern Utah, Microcoleus vaginatus, Nostoc spp. and Scytonema sp. were dominant (Garcia-Pichel and Belnap, 1996). Nostoc commune, Scytonema ocellatum, and Microcoleus vaginatus formed Nostoc-Scytonema communities in steppes and semideserts in the territory of former USSR (Gollerbach and Shtina, 1969).

But in some regions Microcoleus vaginatus and Nostoc commune were not found in biological crusts communities. For example, during the study of cyanobacterial microblotic crusts in eroded soils of а tropical dry forest in the Baja California Peninsula in Mexico, Scytonema cf. ocellatum, Scytonema sp., Microcoleus cf. paludosus, M. cf. sociatus, Calothrix cf. elenkinii, Calothrix cf. marchica, Nostoc cf. microscopicum, and Phormidium sp. were detected (Maya et al., 2002). Possibly, the absence of Microcoleus vaginatus and Nostoc commune is caused by the transitional character of the territory. Microcoleus vaginatus and other cyanobacteria from the order Oscillatoriales usually form a continuous constant film (takyr crusts) in clayey deserts soils of Middle Asia (Gollerbach and Shtina, 1969; Novichkova-Ivanova, 1980).

Microcoleus paludosus, M. vaginatus, and Xenococcus lyngbyae were the most frequent species in microbiotic crusts in the Gurbantunggut Desert in Western China (Chen et al., 2007). During the long-term study of microbiotic crusts on artificially stabilized sand dunes in Tengger Desert, China, a large number of cyanobacteria, including Microcoleus vaginatus, were detected during first stages of dune stabilization after 0–8 years, but these species were not found in stylized dune after 24 years (Li et al., 2002). Together with Microcoleus vaginatus, Anabaena azotica, Limnoraphis cryptovaginata (as Lyngbya cryptovaginata), Jaaginema pseudogeminatum (as Oscillatoria pseudogeminata), Oscillatoria obscura, O. subbrevis, Microcoleus autumnalis (as Phormidium autumnale), Leptolyngbya lurida (as Phormidium luridum), Leptolyngbya tenuis (as Phormidium tenue), Scytonema javanicum, S. millei, and Schizothrix rupicola were also found.

In the dry savannah ecosystem in Boodjamulla National Park in Northwestern Queensland (Australia) filamentous species Sypmplocastrum purpurascens and Scytonema sp. were found to be the dominating species (Büdel et al., 2018).

Using the modern methods of molecular-genetic analysis, huge hidden biodiversity of cyanobacteria in arid regions has been estimated. For example, during the study of soils of the Atacama Desert by 16S rRNA gene cloning/sequencing directly from soil samples and 16S rRNA gene sequencing of clonal cultures, filamentous cyanobacteria Oscillatoriophycideae, Nostocophycideae and Synechococcophycideae were detected. The cloning method revealed 17 taxa, perhaps unsequenced or unculturable. High diversity of phylotypes, possibly new genera and new species were found (Patzelt et al., 2014).

4.2 Temperate Climate

In temperate climate, forest and grassland are the dominant ecosystems. In the territory of Eurasia the grassland are called steppes. Forest steppes are transitional biomes between the forest and steppes (Werger and van Staalduinen, 2012).

The data on biodiversity of cyanobacteria in temperate zones is less numerous. Detailed information on cyanobacteria in the territory of former USSR was published by Gollerbach and Shtina (1969). Information about the biodiversity of soil algae, including cyanobacteria, in all types of forest ecosystems of Eurasia (in the territory of former USSR) were summarized in the book Soil algae of forest biogeocoenoses by Aleksakhina and Shtina (1984). It was found that in forest soils, cyanobacteria are usually very rare. But the biodiversity of cyanobacteria depends on the forest type. Prevalence of cyanobacteria was observed in floodplain soils under oak and pine forests. In forest soils, dominant species of cyanobacteria recorded were Desmonostoc muscorum (as Nostoc muscorum), Nostoc punctiforme, Microcoleus autumnalis (as Phormidium autumnale), and Leptolyngbya foveolarum (as Phormidium foveolarum) (Aleksakhina and Shtina, 1984).

The rarity of cyanobacteria in forest soils was confirmed in other investigations. In the algal flora of limed and unlimed forest soils in the Ardennes (Belgium) only two species of cyanobacteria—Leptolyngbya foveolarum and Microcoleus autumnalis (as Phormidium autumnale)—were detected (Hoffmann et al., 2007). In the soils of the northern part of The Great Smoky Mountains National Park (Tennessee-North Carolina, United States) only Symplocastrum friesii was found (Khaybullina et al., 2010).

In the territory of South Ural region, highest number of species of terrestrial cyanobacteria was detected in the boreal-forest zone (39 species) in comparison with broad-leaved forest (18 species), forest steppe (24 species), and steppe regions (29 species). A number of species, like Aphanothece stagnina, Hormoscilla pringsheimii (Fig. 2F), Leptolyngbya cf. hansgirgiana, Leptolyngbya cf. nostocorum, Kamptonema animale, Kamptonema laetevirens, Oxynema cf. acuminatum, Phormidium aerugineo-caeruleum, Phormidium cf. retzii, Phormidium tergestinum, Phormidium uncinatum (Fig. 2G), and Nostoc cf. ellipsosporum were found only in the boreal-forest zone. cf. Trichocoleus hospitus (Fig. 2H) was the widely distributed species in the broad-leaved forest zone. Myxosarcina cf. tatrica and Chroococcus varius were detected only in this type of ecosystem (Gaysina et al., 2018).

The maximal number of cyanobacteria (14 species) were found in the sample from the road in floodplain forest with Alnus glutinosa (L.) Gaertn. and Padus avium Mill.: Borzia trilocularis, Cylindrospermum majus (Fig. 2I), Cylindrospermum sp., Leptolyngbya foveolarum (Fig. 2J), Leptolyngbya voronichiniana (Fig. 2K), Microcoleus vaginatus (Fig. 2L), Nostoc cf. calcicola, N. cf. punctiforme (Fig. 2M), Phormidium ambiguum, P. breve (Fig. 2N), P. corium, P. dimorphum (Fig. 2O), Roholtiella bashkiriorum, cf. Trichocoleus hospitus, Trichormus variabilis (Fig. 2P) (Gaysina et al., 2018).

Biodiversity of cyanobacteria in forest steppes was also discussed in some previous works (Kuzyakhmetov, 1992; Bakieva et al., 2012). A total of 56 species of cyanobacteria were found in the Tra-Tau and Yurak-Tau Mounts in the forest-steppe zone of Bashkiria. The widest distributed species were Leptolyngbya foveolarum, Phormidium jadinianum, Nostoc punctiforme, Microcoleus autumnalis (as Phormidium autumnale). Possibly, the predominance of cyanobacteria is a result of the calcareous substrate (Bakieva et al., 2012).

In forest-steppe and steppe ecosystems, cyanobacteria often form biological crusts communities. Microbiotic crusts can be found in places without anthropogenic pressure and grazing on the roadside, on small hills, mounts, and on different types of steppes (Bakieva et al., 2012; Gaysina et al., 2018). As already stated above, Nostoc commune, Scytonema ocellatum, and Microcoleus vaginatus create unique cenoses in the arid regions (Gollerbach and Shtina, 1969). In the territory of Bashkiria, Pseudophormidium hollerbachianum and Nostoc cf. commune were abundant in the steppes. It is necessary to note that some species of cyanobacteria, typical for freshwater or humid conditions (Komárek and Anagnostidis, 1999), were detected in this ecosystem. For example, Cyanothece aeruginosa was detected in a forb-grass steppe near Sibay town (Gaysina et al., 2018). Cyanothece aeruginosa was also found in biological crust communities in a sand savanna of Northwestern Ohio (Neher et al., 2003). Possibly, several genotypes of Cyanothece aeruginosa living in different ecosystems also exist.

Using the polyphasic approach, the estimate of hidden biodiversity can be gauged along with serving to provide a correct species identification. For example, during the study of soil cyanobacteria in the territory of South Ural region (Russia) and Joshua Tree National Park (United States) several strains, similar to genus Calothrix by heteropolar tapering trichomes and Nostoc by constricted trichomes with serial arthrospore were isolated (Bohunická et al., 2015b). Careful morphological observation together with molecular-genetic analysis and electron microscopy have revealed that it belonged to a new genus Roholtiella with four species: Roholtiella edaphica, R. bashkiriorum, R. fluviatilis, and R. mojaviensis. This finding confirms that we are still very far from the estimation of real biodiversity of cyanobacteria.

5 Terrestrial Cyanobacteria in Environmental Stress Conditions

5.1 Volcanic Ash

Сyanobacteria is among the first organisms colonizing the lifeless substrates. The role of cyanobacteria in the overgrowing of volcanic substrates is ambiguous, as evidenced by numerous publications.

Important data about cyanobacteria, growing on volcanic ash, were published after the Krakatau volcano eruption in 1883 (Treub, 1888). It was found that filamentous cyanobacteria like Tolypothrix and Anabaena were dominant in the restoration of this type of substrates.

Another model ecosystem for the study of colonization of surface after volcanic activity was Surtsey Island, which was formed in 1963 (Schwabe, 1970, 1974; Schwabe and Behre, 1971; Henriksson, 1971; Henriksson et al., 1972; Brock, 1973). In the first stage of colonization of this island, the number of cyanobacteria species was about 10% of species biodiversity. Cyanobacteria were dominant only near lava flows (Schwabe, 1972). Anabaena variabilis Küzting and several Nostoc Vausher species were detected (Henriksson et al., 1972). After several years the biodiversity increased (Henriksson and Henriksson, 1974) and the number of cyanobacterial cells in 1 g of soil reached 160,000 (Henriksson and Rodgers, 1978; Henriksson et al., 1989).

There are some data about cyanobacteria on the volcanic ash of Kuril-Kamchatka arcs (Shtina et al., 1992). Volcanic substrates near volcanoes Tyatya, Golovina, Mendeleeva (Kunashir Island), Tolbachik (Kamchatka Peninsula) were studied. After the eruption of volcano Tyatya in 1973 the substrate was sterile and nontoxic for cyanobacteria (Kuzyakina, 1983). The most interesting was the crater Otvazhny of this volcano. In 1980, 7 years after the eruption, four species of cyanobacteria were found around the volcanic steam outlet with temperatures of 50–70°C. Among these species was Mastigocladus laminosus Cohn, which usually inhabits the hot springs (Shtina et al., 1992). In 1983, inside the edge of the crater nine taxa were detected: Syneсhocystis aquatilis, Aphanocapsa muscicola (as Microcystis muscicola), Aphanothece castagnei, Mastigocladus laminosus, Nostoc gelatinosum, N. humifusum, Desmonostoc muscorum (as Nostoc muscorum), Oscillatoria geminata f. sulphurea, Leptolyngbya gracillima (as Plectonema gracillimum), and Leptolyngbya (as Plectonema nostocorum). In the volcanic ash of Tolbachik volcano, Nostoc sp. was detected. In the volcanic soil near Golovina volcano, cyanobacteria were not found (Shtina et al., 1992).

The rarity of cyanobacteria in volcanic ash was confirmed in other studies. During investigations of conspicuous algal and cyanobacterial growth in arid steppe on the silt-sized ash after the eruption of Mount St. Helens (Washington state) cyanobacteria were very rare (Rayburn et al., 1982).

In all, 25 species of cyanobacteria were identified in soil microalgal communities of an active volcano on Deception Island (South Shetlands, Antarctica). These groups of organisms were dominant at most sites. Microcoleus autumnalis (as Phormidium autumnale) and Leptolyngbya spp. were the most widespread taxa. These species form mucilaginous structure, which protect other phototrophs from UV radiation and supports the humidity of the substrate. Filamentous cyanobacteria are the taxa that can colonize severe lifeless substrates (Fermani et al., 2007).

During the investigation of bacterial and eucaryotic assemblages associated with fumarolic and nonfumarolic grounds of Socompa Volcano in the arid core of Atacama Desert it was found that cold-fumarole soil hosted communities characterized by cyanobacteria represent 11% of the total number of bacterial and eukaryotic sequences. In these soils, Nostoc relatives were abundant among the Cyanobacteria (Costello et al., 2009).

Cyanobacteria were found in phototrophic cryptoendolithic communities in volcanic glass in Iceland, using fluorescent in situ hybridization (FISH) and 16S rDNA analysis. This data demonstrates that such communities in volcanic rocky environments, protected from ultraviolet radiation, phototrophs, including cyanobacteria, could exist on early Earth (Herrera et al., 2009).

During the study of the diversity of microbial communities in two terrestrial volcanic glasses in Iceland, using metagenomics approach, Actinobacteria were dominant in 16S rRNA gene clone libraries in both sites. But Proteobacteria, Acidobacteria, and Cyanobacteria were also characterized by a high distribution. Interestingly, 15%–34% of the sequenced clones belong to novel microbial taxa. A large number of cyanobacterial clones were very similar to sequences from lithic environments (Kelly et al., 2010).

5.2 Salted Soils

Tolerance of cyanobacteria to high salt concentrations has been discussed in numerous publications. Cyanobacteria were found in arid salted soils (Lund, 1962). Development of blue-green algae with the dominance of Nostoc commune in the highly alkaline usar soil in India was detected by Singh (1950). Cyanobacteria were grown extensively in the wet period on takyr soils with pH 9–10 in deserts of former USSR. Representatives of the genera Microcoleus, Phormidiun, and Nostoc commune (as Desmonostoc commune) were the most abundant species (Gollerbach et al., 1956).

In a study on the influence of different salts on algae and cyanobacteria from salted sails, it was found that the cyanobacteria were the most resistant bacteria. Microcoleus vaginatus crusts started to grow in liquid media after cultivation in salts solutions. This species can grow under the influence of NaNO3, Na2CO3, MgCl2, CaCl2 in concentrations of 0, 5 eq/L, NaCl in concentration of 1 mol/L. Active trichome movement was observed at concentration of NaNO3—0.0625 eq/L, MgCl2—0.125 eq/L, Na2SO4 and NaCl—0.25 eq/L (Bolyshev et al., 1965).

Halophytic solonchaks (salted soils) develop on the coastal plains and in depressions with a close occurrence of saline groundwater. In this kind of ecosystems in the Sahara-Gobi Desert area the representatives of the order Nostocales are widely distributed—Nostoc, Anabaena, Anabaenopsis, Aulosira, Tolypothrix, and Calothrix. In solonchaks of the High Plateau in Algeria cyanobacteria from order Oscillatoriales grow well. Besides, in Pol Gazel region in deep depressions, where higher plants cannot grow, halotolerant cyanobacteria Nostoc humifusum, Anabaena oscillaroides, and genus Aphanothece and Synechocystis were found. In solonchaks in Egypt in the crust along with the prevalence of Schizothrix coriaceae representatives of Nostoc humifusum and Nostoc punctiforme were detected (Novichkova-Ivanova, 1980).

During the study of algae and cyanobacteria of Azovo-Syvashski National Nature Park (Ukraine) in various types of salted soils and vegetation—true-solonchak, meadow-halophilous, saline steppes—49 cyanobacteria species were detected. The most widespread genera were Leptolyngbya, Calothrix, Phormidium, Lyngbya, Jaaginema, Anabaena and Nostoc. Leptolyngbya fragilis, L. tenuis, and Nostoc linckia were the most frequent species. Leptolyngbya fragilis, Phormidium paulsenianum, and Nostoc linckia were found to grow macroscopically on soils covered by meadow-halophilous vegetation (Vinogradova and Darienko, 2008). The authors concluded that cyanobacteria were highly distributed on bare soils and in places with rare vegetation, because they are highly resistant to extreme ecological factors, like high salt concentration, high insolation, and abrupt fluctuations in humidity.

During the study of the biodiversity of soil algae and cyanobacteria of salted soils in steppe zone of Bashkiria (Russia), there types of solonchaks were studied:

1 type—solonetz meadow medium, areas with elevated terrain;

2 type—solonetz meadow medium, areas with depressions;

3 type—solonchak meadow-chernozem, cork-plump with crystals of salts on the surface (Khaibullina and Gaisina, 2008).

Solonchaks have a neutral or alkaline chemistry in which usually the chloride-sulfate type of salinity prevailed.

Chemical analysis of soil samples of 1 type of salted soils showed an increased concentration of Ca² + and Na+ ions with a neutral and slightly alkaline reaction of the soil solution. The base saturation was about 80% (Table 1).

Table 1

Notes: 1—solonetz meadow medium, areas with elevated terrain; 2—solonetz meadow medium, areas with depressions; 3—solonchak meadow-chernozem, cork-plump with crystals of salts on the surface (Khaibullina and Gaisina, 2008).

In this study 33 species of cyanobacteria were found. Leptolyngbya foveolarum (as Phormidium foveolarum), Phormidium paulsenianum, P. jadinianum, and P. breve (as Oscillatoria brevis) developed in all types of solonchaks, Microcoleus autumnalis (as Phormidium autumnale) was typical for both 1 type and 2 type meadow solonetz (Khaibullina and Gaisina, 2008).

5.3 Anthropogenically Disturbed Areas

Cyanobacteria play an important part in the restoration of disturbed areas. It colonizes the lifeless substrate after anthropogenic degradation, including mine spoils. These habitats are characterized by high concentrations of heavy metals, lack of water, high levels of isolation, and deficient nutrient contents (Trzcińska and Pawlik-Skowrońska, 2008).

Algal communities of calamine mine are spoiled with high concentrations of zinc, lead, and cadmium and include several cyanobacteria genera and species: Lyngbya, Oscillatoria, Phormidium, Microcoleus, Nostoc edaphicum. Genus Lyngbya and Nostoc edaphicum are probably the most distributed taxa (Trzcińska and Pawlik-Skowrońska, 2008). In soil algae communities near spoil dumps in Southern Poland with high concentrations rich in Zn, Pb, Fe, Cd, and Tl, cyanobacteria Nostoc sp., Oscillatoria sp., and Phormidium sp. were detected (Cabala et al., 2011).

The taxa Anabaena sp., Pseudanabaena sp., Phormidium sp. were grown as biofilms on the surface of samples from Valenciana (Guanajuato, Mexico) mine tailings during the long-term bioassay (García-Meza et al., 2006).

Cyanobacteria Microcoleus vaginatus, M. autumnalis (as Phormidium autumnale), Nostoc muscorum, N. cf. calcicola and representatives of the genera Leptolyngbya, Phormidium, Pseudophormidium, Schizothrix were detected in reclaimed soils in brown coal and lignite postmining area of Sokolov (Czech Republic) and Cottbus (Germany) (Lukešová, 2001). The genera Microcoleus, Oscillatoria, and Phormidium dominated the spoils of age 1–2 years of Kansk-Achinsk coal deposit (Russia) (Kabirov, 1997). On the spoils of age 5–9 years, algal communities with a prevalence of the genera Pseudophormidium, Phormidium, and Oscillatoria were detected. On all spoils, species from order Oscillatoriales were dominant and consisted 83% of all cyanobacteria species.

In areas of Western North Dakota, disturbed by coal mining, cyanobacteria Nostoc commune was detected in all the studied sites. Phormidium breve (as Oscillatoria brevis), Oscillatoria sp. 1, and Anabaena sp. 1 were also highly distributed species. Microcoleus sp., Lyngbya aestuarii, Cylindrospermum licheniforme, Oscillatoria sp. 2, Nostoc sp., Scytonema hoffmannii, and Plectonema sp. were also found (Starks and Shubert, 1982).

It is necessary to note that mine spoils are inhabited not only by ubiquitous and highly resistant cyanobacteria but also by rare and unique species. During the study of algae and cyanobacteria of mine spoils of Sibay branch of Uchalisnky mining (Russia) in 2010, an interesting strain of cyanobacteria was isolated. Detailed study of this strain using light, transmission electron and fluorescence microscopy, molecular-genetic analysis, high-performance liquid chromatography together with high-resolution mass spectrometry have revealed that it belonged to a peculiar family Gomontiellaceae and was identified as Hormoscilla pringsheimii (Bohunická et al., 2015a). Evaluation of toxins produced by the studied strain revealed the release of the hepatotoxin cylindrospermopsin (CYN) by genus Hormoscilla. It is the first record of CYN production by terrestrial cyanobacteria.

6 Polar Cyanobacteria

The Polar Region comprises the Arctic and Antarctic regions and in total constitutes about 14% of the Earth’s biosphere (Rampelotto, 2014). Even though both the regions have almost similar climatic conditions they are found