Part I
Biology and classification of cyanobacteria
Chapter 1
Cyanobacteria: biology, ecology and evolution
Aharon Oren
Department of Plant and Environmental Sciences, The Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel
1.1 Introduction
The first time I observed a prokaryotic microorganism through the microscope was during my first semester as a biology student in Groningen, the Netherlands, in the end of 1969. During the introductory botany course a young faculty member named Wytze Stam showed me filaments of Anabaena with many heterocysts, hidden within the leaf cavities of the water fern Azolla (see Adams, Duggan and Jackson, 2012 for more information). Later Wytze Stam became a pioneer of molecular systematics studies of cyanobacteria (then called âblueâgreen algaeâ), being the first to apply the technique of DNAâDNA hybridization to elucidate taxonomic relationships between different species (Stam and Venema, 1977).
I consider it a special privilege to have been invited to write the introductory chapter to Cyanobacteriaâan Economic Perspective, considering the fact that I have never worked on economic and biotechnological aspects of cyanobacteria, and that during most of my career my studies concentrated on entirely different types of prokaryotes: anoxygenic phototrophic purple sulfur bacteria during my M.Sc. studies and, later, different groups of halophilic Archaea and Bacteria. Still, the cyanobacteria kept fascinating me, and during several periods of my life I have studied different aspects of this important group of prokaryotes. My Ph.D. studies in Jerusalem centered on the ability of certain cyanobacteria, and in particular a filamentous strain from Solar Lake, Sinai, designated Oscillatoria limnetica, to perform not only oxygenic photosynthesis, but also anoxygenic photosynthesis with sulfide as an electron donor, enabling the organisms to lead an anaerobic life (Garlick, Oren, and Padan, 1977; Oren, Padan, and Avron, 1977; Oren and Padan, 1978). The finding that some cyanobacteria also have well-developed modes of survival in the dark under anaerobic conditions, including fermentation and anaerobic respiration with elemental sulfur as electron acceptor (Oren and Shilo, 1979), showed how well certain members of the group are adapted to an anaerobic lifestyle.
During my later studies of microbial life at high salt concentrations and the adaptations of microorganisms to hypersaline conditions I developed an interest in solar saltern ponds for the production of salt. Along the salinity gradient in the evaporation ponds beautiful benthic microbial mats often develop, dominated by cyanobacteria. One of the most spectacular displays of cyanobacteria I know is within the crusts of gypsum that accumulate on the bottom of saltern ponds with salinities between 150 and 200 g/l: an upper orange-brown layer of Aphanothece-type unicellular species, then a bright dark-green layer of Phormidium-type filaments, below which a red layer of photosynthetic purple bacteria is found. This intriguing and very esthetical system became not only one of my favorite objects for research (e.g., Oren, Kßhl, and Karsten, 1995; Oren et al., 2008, 2009), but also a tool for teaching students about the nature of stratified systems and the influence of different physical and chemical gradients on microbial communities. A brief opportunity to study the microbiology of the hot springs (up to 63°C) on the eastern shore of the Dead Sea in Jordan extended my work on extremophilic cyanobacteria to the thermophiles as well (Ionescu et al., 2009, 2010).
In recent years I became involved in an entirely different aspect of the cyanobacteria: problems connected with the systematics and in particular with the nomenclature of the group. In the course of my activity within the International Committee on Systematics of Prokaryotes I realized that the cyanobacteria are a highly problematic group as far as nomenclature is concerned. On the one hand they were traditionally considered to be plants and their nomenclature was therefore regulated by the provisions of the International Code of Botanical Nomenclature (since 2012: the International Code of Nomenclature for algae, fungi, and plants); on the other hand, they belong to the prokaryotic world and as such their nomenclature may be regulated by the International Code of Nomenclature of Prokaryotes (The Bacteriological Code) (Oren, 2004, 2011; Oren and Tindall, 2005). This led to interesting discussions with the cyanobacterial taxonomists (Oren and KomĂĄrek, 2010; Oren, KomĂĄrek and Hoffmann, 2009). No quick solution of the many remaining nomenclature problems can be expected in the near future.
Thinking about the invitation by the editors of this book to write a chapter entitled âCyanobacteriaâbiology, ecology and evolution,â it is clear that such an introductory chapter can never cover all aspects. I therefore chose to briefly highlight a number of the topics related to the life of the cyanobacteria that fascinate me most.
- Cyanobacteria have been around on our planet for a very long time and they were the first organisms to form molecular oxygen and to change the biosphere from anaerobic to largely aerobic.
- Cyanobacteria are a morphologically diverse group, more diverse than any other group of prokaryotes, and some show unique patterns of cell differentiation.
- Many cyanobacteria have a global distribution, and they are excellent model organisms to investigate questions of microbial biogeography and evolution.
- Cyanobacteria are major contributors to the primary production of the oceans, and they are one of the most important groups that fix molecular nitrogen.
- Cyanobacteria are highly efficient in adapting to their environment; many can actively move toward more favorable areas; they adapt their pigmentation according to the intensity and sometimes also to the color of the available light; some show surprising adaptation toward a life under anaerobic conditions; many types thrive at extremes of temperature, salinity, and pH; and when growth conditions are not suitable, some species can survive adverse conditions for long periods.
- Most types of cyanobacteria are relatively easy to grow in the laboratory, and many have been obtained and studied in axenic culture.
Because of my interest in the history of microbiology, I refer throughout the chapter to the historical aspects of the research, trying to show how different concepts and ideas have developed through time.
1.2 Cyanobacteria are ancient microorganisms
The Precambrian has been termed âthe age of blueâgreen algaeâ (Schopf, 1974), and Schopf and Walter (1982) called the Proterozoic eraâthe period between 2.5 and 0.54 billion years (Ga) ago when the atmosphere turned from anoxic to oxygenated as a result of oxygenic photosynthesisââthe age of cyanobacteria.â
Although there is still considerable controversy about the exact time the cyanobacteria started to appear on Earth, there is be no doubt that they are extremely ancient organisms. There is evidence that oxygenic photosynthesis occurred even in the Archean era (Knoll, 1979; Olson, 2006), possibly even >3.7 Ga ago (Rosing and Frei, 2004). The Precambrian sedimentary record abounds with microfossils that resemble different types of present-day cyanobacteria, and it is generally assumed that the cyanobacteria originated well before 2.5 Ga ago (Schopf, 1970, 1993, 2012; Schopf and Barghoorn, 1967; Schopf and Packer, 1987). Four key rock sequences are known that have survived without major changes in the metamorphosed state from the first billion years (3.8â2.8 Ga) of Archean Earth history:
- the Warrawoona and George Creek Groups of Western Australia, âź3.5 Ga old
- the Onverwacht and associated groups of southern Africa, âź3.5 Ga old
- the Pongola Supergroup of Natal, âź3.1 Ga old
- the Fortescue Group of Western Australia, âź2.8 Ga old (Schopf and Walter, 1982).
The oldest reliable microfossils are those from the Apex chert of northwestern Western Australia and the Fig Tree series of South Africa (3.1 Ga). Some of these, which may or may not have been cyanobacteria, have been referred to as alga-like (Pflug, 1967; Schopf and Barghoorn, 1967; Pflug et al., 1969; Schopf, 1993). But one cannot be certain that such âalga-likeâ unicellular structures were indeed cyanobacteria.
Much has been written about the nature of the Precambrian stromatolitesâlayered rocks that resemble the properties of modern stratified microbial mat communities of cyanobacteriaâand, since their discovery in the 1960s, the microfossils found in them (Barghoorn and Tyler, 1965; Cloud, 1965; Buick, 1992; Grotzinger and Knoll, 1999). There seems to be little doubt about the cyanobacterial nature of microfossils present in stromatolites of the Transvaal sequence (2.25 Ga) (MacGregor, Truswell, and Eriksson, 1974; Nagy, 1974), and biomarkers possibly derived from cyanobacteria (methylhopanoidsâderivatives of 2-methylbacteriohopanepolyolsâwhich occur in many modern species) have been found in organic-rich sediments as old as 2.5 Ga (Summons et al., 1999). Altermann (2007) provided a critical discussion of the different reported claims for the finding of more ancient, 3.8â2.5 Ga-old fossils of cyanobacteria.
The modern stromatolites discovered in the late 1950s in Shark Bay, a slightly hypersaline marine lagoon in Western Australia (Logan, 1961), are often considered as equivalents of the fossil stromatolites that have remained from the Precambrian. These stromatolites have been studied in depth (Bauld, 1984; Stal, 1995, 2012), but it still cannot be ascertained to what extent the communities in Shark Bay indeed resemble the kind of structures built at the time oxygenic phototrophs first colonized the planet and started to release oxygen to the atmosphere.
1.3 Cyanobacteria are morphologically diverse
Cyanobacteria can be defined to include all known prokaryotes capable of oxygenic photosynthesis. Phylogenetically (as based on the small-subunit ribosomal RNA-based tree of life) they ar...