Hydrobiologia (2014) 740:1–11 DOI 10.1007/s10750-014-1971-9 OPINION PAPER Taxonomy of cyanobacteria: a contribution to consensus approach Katarzyna A. Palinska • Waldemar Surosz Received: 4 April 2014 / Revised: 7 July 2014 / Accepted: 7 July 2014 / Published online: 24 July 2014 Ó The Author(s) 2014. This article is published with open access at Springerlink.com Abstract Diversity of Cyanophyceae/cyanobacteria contribute to discussions on the traditional and newly is expressed by their morphological, biochemical and emerging concepts of species and speciation in physiological properties, which enable them to settle prokaryotes. This article reviews the present status and persist in a wide range of habitats. Their diverse of the taxonomy of cyanobacteria, describes earlier, morphology determined their taxonomic distinction classical and recent taxonomic approaches and the based on phenotypic properties. The oxygenic photo- trends for future, emphasizing improvements in synthesis which characterizes cyanobacteria and their methodology as major catalysts for the progress of sharing of ecological niches with eukaryotic algae, this field. prompted their treatment in the phycological circles, where they were called blue-green algae, although Keywords Cyanobacteria Á Phylogeny Á Blue-green their prokaryotic nature, akin to bacteria, has been algae Á Ecotype Á Systematics recognized for over a century. The cyanobacteria are named under Botanical and Bacteriological Codes, and the usage of both systems at the same time causes considerable confusion as the rules of the Botanical Introduction Code are quite different from those of the Bacterio- logical one. Herbarium collections are perfect subjects The history of cyanobacterial systematics has been for intensive phylogenetic studies and therefore can unusually tumultuous. The metabolic property of oxygenic photosynthesis which characterizes cyano- bacteria and their sharing of ecological niches with eukaryotic algae, prompted their treatment in the Handling editor: Stefano Amalfitano phycological circles, where they were called blue- K. A. Palinska Á W. Surosz (&) green algae, although their prokaryotic nature, akin to Department of Marine Biology and Ecology, Institute bacteria, has been recognized for over a century. The of Oceanography, University of Gdansk, main problem in cyanobacterial systematics is that the Al. Pilsudskiego 46, 81-378 Gdynia, Poland e-mail: [email protected] sexual reproduction in cyanobacteria is not known to date. It results in a number of consequences: (i) tradi- K. A. Palinska tional species concepts (Mayr, 1982) cannot be Department of Biology and Environmental Sciences, applied; (ii) strains evolve and undergo evolution; Plant Biodiversity and Evolution Group, Carl von Ossietzky University of Oldenburg, PO Box 2503, (iii) the number of transitional forms and ecotypes is 26111 Oldenburg, Germany numerous (Moore et al., 1998; Rippka et al., 2000); 123 2 Hydrobiologia (2014) 740:1–11 (iv) natural populations differ from cultured strains unquestionably prokaryotes. The basic taxonomic unit which change drastically their morphology under in bacteriological treatment is an axenic-cultured cultural conditions (Palinska et al., 1996). In spite of strain, whereas the species becomes a conceptual it, many important morphologically and ecophysio- construct based on comparison of a number of similar logically stable units exist in nature, and they occur strains. In revising the cyanobacterial genera, Stanier repeatedly in distant localities under similar ecological school relied largely on morphological properties and situations. They are important for ecologists, and thus, used Geitlerian designations, but altered many generic the traditional morphological concept of species is still definitions in accordance with properties expressed in commonly used in ecological studies (Palinska & culture (Castenholz & Waterbury, 1989). In using this Surosz, 2008). approach, many bacteriologists avoid phenotypic Blue-green algae in botanical tradition have been species description. Accordingly, cultured cyanobac- distinguished on the basis of phenotypic properties. teria are usually assigned the name of genus with a Thuret (1875), Bornet & Flahaut (1887, 1888a, b) and strain code. Moreover, bacteriological approach leads Gomont (1892) wrote the first comprehensive taxo- to gross underestimation of the cyanobacteria diver- nomic monographs for blue-greens, recognized by sity in nature. The current edition of the Bergey’s phycologists as a later starting point in taxonomic Manual of Systematic Bacteriology includes compiled referencing. The basic unit of that system is a species information from both bacteriological and phycolog- as defined in botany and zoology (e.g. Mayr, 1982). ical sources (Castenholz, 2001). Geitler (1932) provided an updated taxonomic review Another update and revision of cyanobacterial and determination manual that recognized 1,300 system, which includes ultrastructural properties. is species, classified into 145 genera, 20 families and 3 currently underway (Anagnostidis & Komarek, 1985; orders. Geitler’s work relied on morphology of field- Komarek & Anagnostidis, 1999, 2005; Koma´rek, collected specimens and his classification system 2013). Koma´rek & Anagnostidis (1999, 2005) have marks the beginning of the modern era of cyanobac- developed a formal system being a compromise terial systematics, recognized both by phycologists between Bacteriological and Botanical approaches. and microbiologists. It has formed the basis of Its nomenclature is based on botanical taxonomic numerous revised systems proposed since then, criteria, but it also utilizes bacteriological and molec- including those of Elenkin (1938, 1949), Desikachary ular information. (1959), Fritsch (1959), Starmach (1966), Kondrateva This article reviews the present status of the (1968), Bourelly (1970) and Golubic (1976). These taxonomy of cyanobacteria, describes historical and systems share the view that the systematics of more recent taxonomic approaches and presents the cyanophytes should be based on traditional botanical trends for future, highlighting improvements and criteria, a view sometimes referred to as the ‘‘Geitle- developments in methodology as major promoters rian’’ approach. for the progress of this scientific discipline. In the period 1956–1981, an alternative system was developed by Drouet and Daily (summarized in Drouet, 1981), that drastically reduced the number of Cyanophytes/cyanobacteria under the botanical genera and species of blue-green algae. It was based and the bacteriological codes: a comparison on the hypothesis that the many morphological differences seen in natural samples of cyanophytes Classical taxonomy represents a body of work that has are ephemeral and that numerous ‘‘species’’ of accumulated over past 250 years, since the introduc- cyanobacteria are actually different ‘‘ecophenes’’ of tion of the binominal naming system by Linnaeus in true taxa. However, it was shown that this system does the 1750s. A crucial component of current practice in not reflect the true genetic diversity among blue- taxonomy of cyanobacteria as well as in general greens and was never fully accepted. taxonomy is the concept of the type specimen that Waterbury & Stanier (1977), Krumbein (1979) and serves as the central reference for comparisons. Rippka et al. (1979) proposed that the systematic Designating a type specimen is required when a new treatment of cyanobacteria should be based on bacte- species is named, and these are usually deposited in riological criteria on the ground that they are collections and herbaria. However, the system 123 Hydrobiologia (2014) 740:1–11 3 depends heavily on specialists whose knowledge is approach, species names can be validly published in frequently lost when they are not active any more. any journal, and the existing botanical nomenclatural Today, there are still different ‘‘species’’ concepts information is widely scattered. To establish whether a and definitions in different groups of organisms. There species is novel to science, the literature to be checked are different Codes of Nomenclature guiding the extends over more than a hundred years. In contrast, relationships among taxa. Neither of these rules IJSEM/IJSB is the only platform for bacteriological requires documentation of phylogenetic interrelation- nomenclature. From the situation that two Codes guide ships among taxa, although such background was the taxonomy of cyanobacteria and from the endeav- always desirable. our to come to any compromise of the bacteriological The ‘‘Cyanophytes’’ were traditionally classified as and botanical approaches, several proposals leading to ‘‘blue-green algae’’, with respect to their morpholog- the compatible nomenclatural procedures using the ical diversity and size corresponding to other micro- both Bacteriological and Botanical Codes were pub- algae, as well as to their function in natural biotopes. lished. The important steps in this effort are the Therefore, they were for a long period in the field of compromise proposals of Friedmann & Borowitzka interest of botanists (phycologists) and ecologists, and (1982) and, recently, the corresponding chapters in the treated as microscopic plant organisms. The detailed both editions of Bergey’s Manual of Systematic cytological and biochemical studies performed by Bacteriology (Castenholz & Waterbury, 1989; Ca- bacteriologists on axenic culture strains led to the stenholz, 2001), from which the majority of proposed