Hydrobiologia (2010) 639:231-243 DOI 10.1007/sl0750-009-0030-4
FYTOPLANKTON Review paper
Modern taxonomie revision of planktic nostocacean cyanobacteria: a short review of genera
Jiří Komárek
Published online: 18 December 2009
© Springer Science+Business Media B.V. 2009
Abstract The taxonomy of cyanobacteria has been substantially modified in the last few decades, particularly after application of modern ultrastructural and molecular methods. The group of heterocytous cyanobacteria (Nostocales) was found to be monophy-letic, but the concept and content of different genera must be continually corrected and revised. The widespread introduction of the molecular approach (especially 16S rRNA gene sequencing) has confirmed almost all traditional genera based on distinct and morphologically recognizable type species, but indicated also broader diversity resulting in separation of more genetic and generic entities in several genera. The combination of molecular and phenotype analyses enables also a better and more objective definition of criteria for describing newly researched generic
Guest editors: T. Zohary, J. Padisäk & L. Naselli-Flores / Phytoplankton in the Physical Environment: Papers from the 15th Workshop of the International Association for Phytoplankton Taxonomy and Ecology (IAP), held at the Ramot Holiday Resort on the Golan Heights, Israel, 23-30 November 2008
J. Komárek (El)
Institute of Botany, Czech Academy of Sciences, Dukelská 135, 37982 Třeboň, Czech Republic e-mail: komarek@butbn.cas.cz
J. Komárek
Faculty of Science, University of South Bohemia, Branišovská 35, 37005 České Budějovice, Czech Republic
units, discovered from various habitats in the biosphere. Here, the nostocacean generic taxa are reviewed after recent necessary taxonomic corrections. Nostocacean cyanobacteria are filamentous, heterocytous, not branched and not polarized mor-photypes, classified traditionally into one family (Nostocaceae). The main part of the review focuses on the genera containing planktic species.
Keywords   Cyanobacteria • Taxonomy • Ecology • Molecular evaluation • Phenotype characteristics • Plankton • Generic concept
Introduction
All heterocytous cyanobacteria represent a monophy-letic clade according to molecular evaluation (Fig. 1; Giovannoni et al., 1988; Wilmotte & Golubič, 1991; Turner, 1997, 2001; Castenholz, 2001; Rajaniemi et al., 2005a, b, etc.). The only exceptions are several non-heterocytous types, which were earlier classified as coccoid types with a complicated and differentiated thallus (e.g. several strains of Chroococcidiopsis). Their phylogenetic position among heterocytous types must be studied and explained in the future. Molecular sequencing appeared to be particularly important for determining phylogenetic relations among various genera, which represent distinct taxonomic units in the spectrum of cyanobacterial diversity.
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Subclusters inside the clade of Nostocales (e.g. on the level of taxonomic families) were re-defined according to the genetic investigations and, subsequently, re-evaluated morphological features. The nostocalean cyanobacteria form more or less complicated filaments. They are very unique bacteria, where the individuals have a multicellular, diversified thallus with prominent cells of different function (heterocytes, akinetes and necridic cells). Therefore, the morphology and revision of the value and variability of cytomorphological features play an important role in their characterization. As other cyanobacteria, they contain the complete photosyn-thetic system and ecologically they belong among microscopic plants. Of the morphological characters, the type of branching appears especially important. Gugger & Hoffmann (2004) confirmed that false and true branching cannot be a distinguishing character between two phylogenetic clades, but the branching type can be characteristic for different subclusters inside Nostocales (usually classified as families; Hoffmann et al., 2005; Fig. 2).
The family Nostocaceae represents a special phylogenetic line and group, which is characterized morphologically by (i) isopolar filaments, (ii) the absence of any branching (with the exception of certain anomalies), (iii) the presence of heterocytes (with the exception of secondary derived genotypes) and (iv) the facultative presence of typical parahet-erocytic or apoheterocytic akinetes (which do not develop in other heterocytous clades; the resting or dormant cells are of another type). Taxonomic changes on the generic level in nostocacean cyanobacteria are summarized in the present review. These changes were proposed to the end of 2008 on the
traditional STIGONEMATALES
Fig. 2 Various types of true branching (Anagnostidis & Komárek, 1990), considered in traditional taxonomy as the characteristic feature of the order Stigonematales. All the genera with true branching are not monophyletic, and different types of true branching are characteristic for separate clades and distinct families (Gugger & Hoffmann, 2004). A irregular, B T-like branching (uniserial and multiserial trichomes— different examples), C Y-like branching, D reverse Y-like branching. Small letters (a-k) indicate various subtypes
basis of combined molecular, cytological and morphological studies of the diversity of this cyanobac-terial group.
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Methods
The results presented in this article are a compilation of taxonomie results, published in numerous papers and based mainly on molecular 16S rRNA gene sequencing, which is considered a more or less standard method for characterization of cyanobacterial genetic and generic units. However, according to the combined polyphasic approach, all results from sequences of other genomes and corresponding cytomorphological, ecophysiological and biochemical markers are important and should also be taken in consideration.
Morphological characteristics are important for practical use and identification of natural populations. The main phenotype character conforming with phy-logenetic clusters (genera) inside of Nostocaceae is a metameric, symmetric or subsymmetric structure of trichomes resulting from the heterocyte and akinete position (para- and apoheterocytic development of akinetes) (Fig. 3; comp. Komárek & Anagnostidis, 1989). Both botanical and bacteriological nomencla-toric rules were respected throughout the whole review.
Revised nostocacean genera (state 2009)
The list of revised generic entities after the commonly used Geitler's (1932) monograph is given in Table 1. In the present review of generic units occurring in planktic environments, those genera not confirmed by 16S rRNA gene sequencing are marked with an asterisk (*). The reference strains are cited according to Castenholz (2001) or the authors of the corresponding genera.
1. Raphidiopsis Fritsch et Rich 1929
[type  species — R. curvata;  reference  strain not
selected]
Unclear and polymorphic genus, containing probably several morpho- and genotypes. The main diacritical character is the absence of heterocytes. Up to now, it has not been confirmed whether the genus is only a non-heterocytous stage of other genera (Cuspidothrix, Cylindrospermopsis). Two strains were sequenced by Li et al. (2008) and their narrow, phylogenetic affiliation to Cylindrospermopsis was demonstrated. However, the identity of both genera is not yet doubtless, and study of more strains is necessary.   Other   characters:    solitary floating
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Fig. 3 Scheme of trichome structure [in relation to position of heterocytes (circles) and akinetes (A)] in main nostocacean genera. The trichome structure is in coincidence with the genetically limited genera [from Komárek & Anagnostidis (1989) and Komárek (2008)]
trichomes, narrowed ends of subsymmetric trichomes, presence of paraheterocytic (solitary or in pairs) akinetes. Five recognizable species and a few unclear morphotypes were described. The most recognized are Raphidiopsis mediterranea Skuja 1937 and the tropical species R. curvata Fritsch et Rich 1929; less known are R. indica Singh 1942, R. sinensis Jao 1951 and R. turcomanica Kogan 1967, named after the country of their occurrence. Other taxa, e.g. R. long-isetae Eberly 1966 and R. brookii Hill 1972, are considered as problematic (Fig. 4A).
2. Cuspidothrix Rajaniemi et al. (2005a)
[type  species — C. issatschenkoi,  reference strain
OTU37s7—Rajaniemi et al., 2005b]
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Table 1   List of generic entities of the family Nostocaceae (Nov. 2008)				
	1	2	3	4
Raphidiopsis Fritsch et Rich 1929	X	X		
Cuspidothrix Rajaniemi et al. 2005	X		x	
Cylindrospermopsis Seenaya et Subba-Raju 1972	X		x	
Aphanizomenon Morren ex Bornet et Flahault 1888	X	X	x	
Anabaena subg. Dolichospermum Thwaites ex Wittrock et Nordstedt 1889	X		x	x!
Anabaena-liks cluster A (Sphaerospermum Zapomělová et al. 2010)	X		x	x!
Anabaena-liks cluster B	X			x
Anabaena-liks cluster C	X			x
Anabaenopsis (Woloszyňska) Miller 1923	X	X	x	
Cyanospira Florenzano et al. 1985	X		x	
Anabaena Bory ex Bornet et Flahault 1888		X	x	
Hydrocoryne Schwabe ex Bornet et Flahault 1888		X		
Aulosira Kirchner ex Bornet et Flahault 1888		x!		
Macrospermum Komárek 2008		x		
Cylindrospermum Kützing ex Bornet et Flahault 1888		x	x	
Cylindrospermum-Xiks, cluster A	00			x!
Wollea Bornet et Flahault 1888		x		
Nodularia (Mertens in Jürgens) ex Bornet et Flahault 1888	00	x	x	
Richelia J. Schmidt 1901	Endoph.	x		
Isocystis (Borzi) ex Bornet et Flahault 1888		x!		
Trichormus (Ralfs ex Bornet et Flahault) Komárek et Anagnostidis 1989			x	
Trichormus-liks cluster A				x
Nostoc Geoffrey ex Linnaeus ex Bornet et Flahault 1888		x	x	
Mojavia Řeháková et Johansen 2007			x	
1 = genera with planktic species, 2 = traditional genera (Geitler, 1932) or described only by morphological characters, 3 = genera described or confirmed by polyphasic approach (molecular and morphological delimitation), 4 = phylogenetic clusters, not validly described, ! = not yet published, but will be validised (also by 16S rRNA gene sequencing) during 2009
Originally classified to Aphanizomenon, from which it can be separated both genetically and morphologically (Rajaniemi et al., 2005a, b; Komárek and Komárkova, 2006; Fig. 5). Morphological diacritical features are solitary, narrow trichomes with subsymmetric structure, paraheterocytic akinetes situated on both sides or slightly distant from hetero-cytes, facultative aerotopes (groups of gas vesicles), and narrowed, elongated and ipointed terminal cells (Fig. 4B). Five species have been described (up to now only the type species Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al., 2005, has been sequenced). Another rare species from East Europe is C. elenkinii (Kiselev) Rajaniemi et al. (2005), and from tropical regions C. tropicalis (Horečka et Komárek) Rajaniemi et al. (2005) and C. capricorni (Cronberg et Komárek) Rajaniemi et al. (2005) (both with akinetes
joined to heterocytes). C. ussatschevii (Proskina-Lavrenko et Makarova) Rajaniemi et al. (2005) has been recorded only from the Caspian Sea.
3. Cylindrospermopsis Seenayya et Subba-Raju 1972 [type species — C. raciborskii, reference strain AWT205]
Originally classified in the genera Anabaena (habitual similarity) or Anabaenopsis (similar type of heterocyte development), but this genus was placed into a separate generic unit according to the subsymmetric, solitary floating trichomes and development of heterocytes only from terminal cells (after asymmetrical division) (Fig. 4C). This separation was confirmed by 16S rRNA gene sequencing, but up to now only strains of Cylindrospermopsis raciborskii have been analysed (Fig. 5). Akinetes develop subterminally,
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B
Solitary trichoma
Absence of hetcrocytes
Solitary trichomas * Pointed apical cells • lniercalar hetcrocytes
: 4
|—or/
9
Solitary trichomes Terminal hetcrocytes
Tendency to fascicutaiion Elongated, hyaline terminal cells Intercalar heierocytes
Solitary trichomes Narowed terminal cells
Spherical ak mutes at heicrocyles
• Solitary trichomes
• Narrowed ends
• Akineles distant from heteroevtes
Fig. 4 Comparison of generic characters of planktic nostoc-acean types with filaments with more or less narrowed ends (only the main diacritical markers are added in the table): A  Raphidiopsis,   B   Cuspidothrix,   C Cylindrospermopsis,
D Aphanizomenon, E Anabaena like cluster A {Sphae rasper-muni), F AnabaenalAphanizomenon like cluster B (drawings selected from various authors)
planktic Anabaena and Aphanizomenon cluster
J
Nodularis
Trichormus
planktic Anabaena and Aphanizomenon
bsnt. Anabaena Cuspidothrix
Cyanospha
Cylindrospermopsis bent. Anabaena
Cylindrospermum
PCC 7203 (28279)
Fig. 5   Part of a phylogenetic tree from Rajaniemi et al. (2005). Distinctly separated genera with planktic species are in the tree
aerotopes occur facultatively in cells. The type species produces toxins and seems to be expanding geographically in recent years. Since the middle of the twentieth
century, it has expanded from its original tropical regions into subtropical and temperate areas. Gugger et al. (2005) discovered a genetic divergence of the
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expanding C. raciborskii. The fact that the majority of 11 morphospecies described were published after 1991 confirms the expulsive development of this genus in recent decades. From the 11 morphospecies described, 9 are known only from tropical habitats. The lists and characteristics of described species are reviewed in papers of Komárek & Komárkova (2003) and Couté & Bouvy (2004).
4. Aphanizomenon Morren ex Bornet et Flahault 1888 [type species — Aph. flos-aquae; reference strain PCC7905]
Planktic heterocytous cyanobacteria with more or less straight trichomes and slightly narrowed or elongated terminal cells were classified traditionally into this genus. Modern genetic and morphological studies restricted the genus in a well-defined cluster of morphospecies, which all have subsymmetric structure of trichomes, a tendency to aggregate straight trichomes in parallel fascicles and which do not have distinctly narrowed ends. The terminal cells are cylindrical, elongated and hyaline in well-developed mature filaments, but not or only very slightly narrowed. All other types with narrowed ends and non-cylindrical, elongated end cells must be classified in other genera (Fig. 4D). The revised genus contains eight morphospecies, which also differ slightly in their ecological demands. The most common and important are A. flos-aquae Ralfs ex Bornet et Flahault 1888, A. klebahnii Elenkin ex Pechar 2008 and A. yezoense Watanabe 1991, which all are distributed only in temperate zones. Other species occur only in isolated areas, but no Aphanizomenon species occurs in tropical regions (Komárek & Komárkova, 2006). There are ecologically and toxicologically interesting types forming water blooms in eutrophic stagnant waters.
5. Anabaena subg. Dolichospermum Thwaites ex Wittrock et Nordstedt 1889
[type species — An. flos-aquae Brébisson ex Bornet et Flahault, reference strain PCC9332]
This genus contains a group of planktic members of the traditional Anabaena, characterized by solitary free-floating trichomes (or living in clusters), and by cells with gas vesicles (forming aero topes). Genetically, this genotype is clearly differentiated from the group of benthic, metaphytic or periphytic species, based on the type species A. oscillarioides. The
phylogenetic separation was confirmed by Iteman et al. (2002), Gugger et al. (2002a, b), Rajaniemi et al. (2005a), Willame et al. (2006) and others (Fig. 5). The morphospecies are more or less recognizable in natural populations, but they have transient features in cultures. Of the traditional characters, particularly coiled or straight trichomes and type of coiling (used mainly for the separation of species) are not stable under culture conditions (Zapomělová et al., 2008). On the contrary, position and form of akinetes, morphology of terminal cells and (in certain limits) size and form of cells seem to be stable for different morphospecies (Fig. 6A). The genus contains about 45 planktic species after revision. For the lists and morphological descriptions see Komárek (1999) and Komárek & Zapomělová (2007, 2008). The validation of the genus Dolichospermum was published recently (Wacklin et al., 2009).
6. Anabaena-like cluster A (Sphaerospermum Zapomělová et al., 2010)
[type species — S. reniforme, reference strain: 06(FM161348)—Zapomělová et al., 2010]
This cluster contains one part of the planktic AnabaenalDolichospermum cluster, which was phy-logenetically distinctly separated from other Dolichospermum types (Zapomělová et al., 2010; Fig. 7). The newly defined genus is morphologically characterized by solitary (coiled or straight), free-floating trichomes, the obligatory presence of gas vesicles, slightly modified terminal cells and the position of spherical akinetes on both sides of heterocytes (Fig. 4E). It contains three species with uncommon and dispersed distributions, Sphaerospermum aphanizomenoides (Fořti) Zapomělová et al. (2010), S. kisselevianum (Elenkin) Zapomělová et al. 2010 and S. reniforme (Lemmermann) Zapomělová et al. (2010).
7. *Anabaena-Y\k& cluster B
[type species and reference strain not selected]
This group contains planktic filamentous and heterocytous cyanobacteria, characterized by floating, solitary, more or less straight or slightly flexuous, metameric trichomes, usually slightly narrowed towards the ends and with elongated akinetes in a paraheterocytic position (Fig. 4F). They were described partly as Aphanizomenon (terminally narrowed cells) or Anabaena (similarity with planktic straight "Anabaena"  species). The cells contain
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B
SoHlary Irichoincs Parahelerocylic akinines
Metameric trichomes
Cylindrical trie homes Qv\h distinctly longer than wide Metamcrio inchomes.
Mctamťric trichomes Special strategy in heterocyte development Paraherelpcytiq ak metes
Metamcrie trichomes Apoheterocytic formation of akineles
* Subsym metric tnchomes
* Special type of helerocyle formatioTi
* Short filaments
Metamcrie trichomes Apoheterocytic formation of akineles Cells state* than wide
Fig. 6 Comparison of generic characters of planktic nostoc-acean types with filaments with not narrowed or elongated end cells (only the main diacritical markers are added in the table): A Anabaena subg. Dolichospermum, B Anabaena-like cluster
C, C Anabaenopsis, D Cyanospira, E Cyalindrospermum-like cluster A, F Nodularia (drawings selected from various authors)
Fig. 7   Phylogenetic tree separating the cluster of Sphaerospermum from other Anabaena-like species (Zapomelova et al., 2010)
ptanktonic Anabaena spp. + Aphanizomenon spp. (54 OTU's); incl. An. compacts (FM161347)
An. osctllarioides BECID32 (AJ630427)
Cuspidothrix (Aph.) issatschenkoi (4 OTU's)
Thchormus variabilis (2 OTU's)
An. augstumalis SCMIDKE JAHNKEMa (AJ630458) An. oscitlarioides BO HINDAK 1984/43 (AJ630428)
Nostoc sp. 152(AJ133161) An. ue/pw(AF160256) Aph. ovalisporum FAS-AP1 (EU076457)
Anabaenopsis sp. + Cyanospira rippkae (3 OTU's)
ijfä/75l An. kisseleviana TAC34 (AY701558) 7B/75n An. kisseleviana NIES74 (AY701557) 99/99
An. renlformls 06-01 (FM161348) An. renlformls 07-01 (FM161349) Aph. aphanlzomenoides 04-43 (FM161350)
Cylindrospermopsis raciborskii (7 OTU's) Synechococcus sp. 0tu28s07 (AM259221)
facultative or obligatory gas vesicles, with the exception of the end cells. More than 20 known morphospe-cies belong to this group. They surely do not belong to Dolichospermum or Aphanizomenon according to genetic investigations, and the determination of several genetic clusters within this group is possible: Aphanizomenon gracile (Lemmermann) Lemmermann 1907, Aphanizomenon skujae   Komarkova-Legnerova et
Cronberg 1992, Aphanizomenon ovalisporum Forti 1911, Aphanizomenon manguinii Bourrelly 1953, Anabaena minderi Huber-Pestalozzi 1938, Anabaena bergii Ostenfeld 1908, and others (cf. Komárek & Kováčik, 1989; Komárek & Komárkova, 2006).
8. *Anabaena-likQ cluster C
[type species and reference strain not selected]
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Another group of planktic, nostocacean types with metameric, solitary, straight or flexuous, rather narrow (1.5—4(7) um wide) trichomes and elongated cells, obligatory with gas vesicles, and elongated, paraheterocytic akinetes distant from heterocytes (Fig. 6B). These types do not belong to any revised genera, but they were not yet evaluated by molecular methods and sequencing. Four morphospecies from northern, oligotrophic or mesotrophic lakes, described as various species of "Anabaena" (A. el-liptica Lemmermann 1898, A. levanderi Lemmer-mann 1906, A. miniata Skuj a 1956, A. tenericaulis Nygaard 1949) and possibly also two little known species from central Asia (A. abnormis Proškina-Lavrenko 1968, A. attenuata Kiselev 1940) belong to this morphological cluster.
9. Anabaenopsis (Woloszynska) Miller 1923 [type species A. elenkinii; reference strain PCC9420] The type species was described originally in 1912 as planktic Anabaena by Woloszynska, but was later classified as a special subgenus and genus by Miller 1923 based on one unique character: The trichomes are metameric, but the heterocytes develop in a specific way (two intercalar neighbouring cells divide synchronously and asymmetrically with smaller daughter parts oriented one to another; from these two smaller cells develop mirror-like unipored heterocytes oriented by pores to trichomes). Trichomes between heterocytes disintegrate later and short trichomes with apical heterocytes arise from this process (Komárek & Anagnostidis, 1989; Figs. 6C, 8). The trichomes are Anabaena-like, solitary, free-floating cells with obligatory or facultative aerotopes. The genus is clearly defined phenotypically and has been confirmed by sequencing (Fig. 9). About 20 morphospecies are described, which differ slightly ecologically. The majority of the species prefer alkaline or slightly saline inland waters. The differential morphological features between species are mainly the width and shape of cells, but numerous transitional types exist (Komárek, 2005). The genus is mainly distributed in tropical and subtropical regions; only a few types occur in temperate zones. The various species develop massive populations (in the form of water blooms). The various morphospecies appear rarely only in cultures, but the separate genetic cluster was confirmed (Iteman et al., 2002; Rajaniemi et al., 2005a; Figs. 5, 9).
10. Cyanospira Florenzano et al., 1985
[type species: C. rippkae; reference strain MAG II 702]
Described according to molecular sequencing (Florenzano et al., 1985; Iteman et al., 2002; Figs. 6D, 9). It is genetically related to Anabaenopsis and Nodularia, however, habitually is similar to coiled planktic Anabaena types (=Dolichospermum). Diacritical markers are (besides phylogenetic position) solitary, free-floating, coiled and metameric trichomes with a facultative occurrence of gas vesicles and apoheterocytic formation of akinetes. Two species were described from Africa (Cyanospira rippkae Florenzano et al. 1985 and C. capsulata Florenzano et al., 1985). "Anabaena" globosa Hir-ano, described from Nepal, also morphologically corresponds to this genus.
11. Cylindrospermum-like cluster A
[type species and reference strain not selected]
This cluster contains a few morphospecies with a special intercalar development of the heterocytes. One vegetative, barrel-shaped and intercalar cell changes its form into a narrower, cylindrical and more elongated proheterocyte, which divides into two parts, from which two heterocytes develop. The trichome later disintegrates between them (Hindak, 2000). From this process, short trichomes with heterocytes in an apical position develop; this stage habitually resembles Cylindrospermum, Anabaenopsis or Cylin-drospermopsis, but the different origin of the heterocytes (connected with the subapical origin of akinetes) indicates a special generic entity (Fig. 6E). Three well-recognizable species with these characteristics were described up to now under different generic names: Anabaena siamensis Antaricanonda 1985 from a rice field in Thailand, Richelia sp. in Hindak, 2000 from the metaphyton of pools in Slovakia and Cylindrospermum planctonicum Cronberg, 2003 from plankton of the Baltic Sea. The taxonomic position of this type can be solved only by molecular studies (cf. Hindak, 2000; Cronberg, 2003).
12. Nodularia (Mertens et Jtirgens) ex Bornet et Flahault 1888
[type species: N. spumigena; reference strain: PCC9350]
This genus was described on the basis of a common habitual appearance of trichomes with short
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239
Fig. 8 Morphological characteristics of Anabaenopsis in comparison with related genera Anabaena and Nodularia. The review of cell form in Anabaenopsis is described in the lower part of the figure [from Komárek & Anagnostidis (1989), Hindák (2001) and Komárek (2005)]
ANABAENA. NCSlJLARIA
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ANABAENOPSIS ""if"! *•
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,— Amitiaeiiapsis PCC 9216 ILO- Atttibaenopsis PCC 9215
100
J    L Atiabuenopsw PCC 9608 ss i—- Atiabaettopsis etenkinii PCC 9420
Crariaspira capsulata PCC 9502 Cyumtspint vippkue PCC 9501
!\in/ufiiria sp. PCC 9350
- Aphunizomciion Jhts-uqttin? PCC 7905
100_lAnahacnaßos-aquae PCC 9349
LfnuAafj/ii flos-aquae PCC 9332 I Anuhuciw fltis-aquai: PCC 9302
AmrorPCC 7120
Fig. 9 Comparison of the phylogenetic position of the genera Anabaenopsis, Cyanospira, Nodularia and Aphanizomenon [according to Iteman et al. (2002)]
(discoid) cells and irregular apoheterocytic formation of akinetes (Fig. 6F). It is the only genus in which the species with gas vesicles were (according to present
knowledge) not genetically separated from morpho-species, which never form gas vesicles and never grow in plankton. Particularly, the planktic species prefer brackish and slightly saline water habitats, but they occur in very separated and distant localities. Planktic species are mostly known from the Baltic Sea (where they form heavy water blooms). Other recent localities are the Caspian Sea, several lakes near the western coast of North America, volcanic lakes in Mexico, coastal lakes in Uruguay and sea bays in SW Australia. All these populations are classified near N. spumigena (or like species), but preliminary genetic analyses indicate that there are specifically different. They differ slightly (but distinctly) also morphologically, e.g. the coiled filaments of N. spumigena occur only in populations
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from the Baltic Sea. Four to five morphospecies were described on the basis of morphological criteria. The populations from the Baltic Sea were already studied several times by the molecular methods (Bolch et al., 1996; Hayes et al., 1997; Bolch & Blackburn, 1998; Lehtimaki et al., 2000), but these results did not agree one to another. The species concept of Nodularia and their diversity must therefore be studied further. A review of 8-10 benthic Nodularia species is simpler, and the morphospecies are easier characterized.
The family Nostocaceae contains the following genera, which only exceptionally occur in planktic habitats. They probably do not have genes for gas vesicle production:
- Anabaena Bory ex Bornet et Flahault 1888— Type species is A. oscillarioides. Confirmed by molecular sequencing (Gugger et al., 2002a, b; Rajaniemi et al., 2005a, b; Willame et al., 2006). It contains only non-planktic (benthic, periphytic, metaphytic, edaphic) morphospecies, and gas vesicles never occur in cells. About 60 described and well-defined morphospecies. They possibly will be divided into more genetic clusters and separated into various genera.
- *Hydrocoryne Schwabe ex Bornet et Flahault 1888—Defined only by morphological criteria, not yet studied by molecular methods. However, few morphospecies are known and repeatedly recorded. Confirmation of generic status and importance of morphological markers is desirable.
- Aulosira Kirchner ex Bornet et Flahault 1888— About 25 morphospecies were described, mostly from tropical aquatic habitats. Main diacritical features are apoheterocytic formation of akinetes and firm sheaths around Anabaena-like trie-homes. Confirmed by molecular methods (but not the type species; Lukešová et al., 2009); the existence of one or a few generic units inside this morphotype is probable (Geitler, 1932).
- *Macrospermum Komárek, 2008—Four tropical species. Originally classified with Anabaena, but morphologically clearly separated by symmetrical trichomes and the special morphology of large akinetes. Metaphytic species, but with facultative gas vesicles. Confirmation by sequencing is necessary.
- Cylindrospermum Kiitzing ex Bornet et Flahault 1888—A morphologically unique, well-defined
traditional genus, which has been confirmed by molecular analyses. Approximately 35 recognizable morphospecies (Geitler, 1932; Bourrelly, 1970; etc.).
- *Wollea Bornet et Flahault 1888—A poorly known genus, which is not yet sequenced with certainty. Morphologically distinct (Desikachary, 1959; Bourrelly, 1970), molecular support is desirable. About six morphospecies were described, mostly from tropical regions.
- *Richelia J. Schmidt 1901—Interesting oceanic genus with 1-2 morphospecies, living endophy-tically, mainly within frustules of planktic diatoms (see, for example, Desikachary, 1959). Not yet confirmed by molecular evaluation, but existence of its genetic homogeny is highly probable. The later classification of three ecologically and morphologically different freshwater species into this genus (Hindák, 2000) is questionable.
- *Isocystis (Borzi) ex Bornet et Flahault 1888—A poorly known genus with about four to eight species. Without heterocytes and with atypical nostocacean akinetes. Classification in the family Nostocaceae is therefore improbable, it must be studied by molecular methods (Komárek & Anagnostidis, 1989).
- Trichormus (Ralfs ex Bornet et Flahault 1888) Komárek & Anagnostidis, 1989—A well-defined and genetically confirmed genus with apoheterocytic formation of akinetes. The genus with about 40 (mostly tropical) morphospecies is based on the commonly distributed soil type species T. {"Anabaena") variabilis, which yields commonly used laboratory model strains. Important N-fixing types belong to this genus. A few other genetically diversified clusters may appear in the genus (Desikachary, 1959; Rajaniemi et al., 2005a).
- Trichormus-like cluster A—Represented by one thermophilic species, which is morphologically similar to the typical Trichormus, but belongs genetically to a separate, not taxonomically validated cluster (Kaštovský & Johansen, 2008).
- Nostoc Geoffrey (ex Linneaus) ex Bornet et Flahault 1888—Very wide and heterogenic cluster, which will surely be divided into several genetic units (Hrouzek et al., 2005). Up to now, about 60 recognizable (many unclear) morphospecies and strains were described. Genetic diversity is wide and must be investigated by
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the help of combined molecular and phenotype methods.
- Mojavia Řeháková et Johansen 2007—A monospecific genus described from American desert soils by combined molecular and morphological methods. From the vicinity of a complex cluster of Nostoc; up to now the only defined cluster, with one species, separated from this genus (Řeháková et al., 2007).
Conclusions
The taxonomie classification of Cyanobacteria must be substantially changed. The introduction of molecular and other modern methods corrected our knowledge of phylogenetic relations of different types of cyanobacterial taxa, which were evaluated up to now mostly on the basis of morphological characters. Populations from geographically and ecologically distant ecosystems were found different by numerous markers, and also the importance and hierarchy of morphological features must be re-evaluated. However, the morphology and morphological variability is important part of the diversity and diversification processes in cyanobacteria in all ecosystems over the world. The complex and combined studies containing both the modern molecular procedures and detailed morphological, ecological, cytomorphological and biochemical studies are also indispensably necessary to the knowledge of the cyanobacterial diversity.
The process of the reorganization of nostocacean taxonomie system was already initiated. The orientation in all changes, which must be in evaluation of cyanobacterial diversity respected, is not easy, particularly for the users of the system, ecologists and experimental researchers. This review is therefore the summarized information about the main changes in nostocacean diversity, which were already published to the end of 2008. Of course, the further corrections and modification are expected already in next few years.
Acknowledgements This work was supported by grants GA AVCR No. IAA600050704 and GA CR 206/08/0318. The author thanks J. Kaštovský, J. Komárkova and E. Zapomělová for their help with the preparation of this presentation and manuscript. This study was presented as an invited paper at the Bat Sheva de Rothschild seminar on Phytoplankton in the
Physical Environment—The 15th Workshop of the International Association of Phytoplankton Taxonomy and Ecology (IAP)—held in Ramot, Israel, November 23-30, 2008.
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Author Biography
Jiří Komárek (b. 1931) is Emeritus Professor of Botany and Phycology at the Faculty of Sciences, University of South Bohemia, České Budějovice, and member of the scientific staff at the Institute of Botany of the Academy of Sciences of the Czech Republic in Třeboň, Czech Republic. He obtained his PhD at the Charles University in Prague and worked in several institutes of the
Czech Academy of Sciences over many years. After 1982, he
worked at several abroad universities and institutions (in Canada, Japan, Mexico and Brazil). In 1991, he participated in the foundation of the University of South Bohemia and he worked as professor of this institution. His scientific interests are focused on taxonomy, ecology and biology (cytology) of microalgae, especially of green algae and cyanobacteria. He is the author of the world monograph of coccoid green algae (1983) and cyanobacteria (1998, 2005). In recent years, he interested mainly in problems of cyanobacterial diversity and diversification and in problems of genetic and phenotypic relations and variability in cyanobacteria.
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