Cells, Cell Division, Trichome Morphology 7
Phenotypic Characters of
Heterocytous Cyanobacteria
Cells, Cell Division, Trichome Morphology
The structure of cells in heterocytous cyanobacteria does not differ substantially
from simpler types. The prokaryotic character, composition of cell wall and presence of basic intracellular structures has more or less the same schema, and differences are mainly in their distribution and localization. Anomalous and specific
structures are sometimes described, but their function and relation to phylogenetic
diversification is still poorly known.
The morphology of cells is variable, but the cell shape (cylindrical, barrel-shaped,
irregular, etc.) is characteristic for different clades (in certain limits), which can
represent also different genera. Phylogenetic analyses confirm that various lineages
contain the main modifications, with only one type of cell morphology (e. g., Nostoc, Aphanizomenon, Scytonema, Anabaenopsis, etc.).
The cells are connected in all heterocytous types into filamentous formations (unsatisfactorily called “trichomes” in the cyanobacteria, as they have no relationship
to trichomes in vascular plant morphology). Cells in cyanobacterial trichomes are
connected by microplasmodesmata (one or more pores in shared septa), distinctly
simpler than plasmodesmata of vascular plants (cf. Fig. 8). Because of these connections, it is necessary to consider the trichomes of cyanobacteria to be individual,
multicellular organisms. In filamentous, heterocytous orders various modifications
of trichomes occur. They can be obligately uniseriate with cells dividing only perpendicular to the long axis of the trichome, or multiseriate, with the ability of cells
to divide in other directions with respect to the lengthwise axis of the trichome. The
uniseriate or multiseriate trichomes are characteristic for various clusters, which
can be classified as different families. However, the morphology of trichomes,
which is considered as important for identification in morphologically complicated
types, can be influenced significantly by environmental factors (e. g., when cultured
under unusual conditions).
Cell division proceeds in almost all filamentous cyanobacteria (including heterocytous types) by centripetal binary fission, in uniseriate trichomes only perpendicularly
to the long axis of the trichome, in polyseriate trichomes in two planes or irregularly
(Geitler 1932, 1960, Drews 1973, Schirrmeister & al. 2011, 2013). Cell division in
several more complicated and diversified genera (in the historical order Stigonematales) is irregular (Thurston & Ingram 1971, Drews 1973, Rippka & al. 1979, 1981,
Nierzwicki & al. 1982, Rippka & Herdman 1985, Rippka 1988). The division of
cells in various planes varies often irregularly and this process can result in various
multiseriate forms of trichomes in various types of true branching. The irregular cell
division in forms with multiseriate trichomes can be slightly modified and different
from the simple trichal, non heterocytous types. Results of these specific types of
cell division are, e. g., the so-called “pit-connections” between cells (see also p. 63),
J. Komárek, Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota,
DOI 10.1007/978-3-8274-2737-3_2, © Springer-Verlag Berlin Heidelberg 2013
8 Phenotypic Characters of Heterocytous Cyanobacteria
Fig. 3. Meristematic zones in isopolar and heteropolar trichomes of representative
nostocalean cyanobacteria; H – heterocytes. (From © Komárek & Anagnostidis 1989)
or the formation of perpendicular rows of cells in multiseriate trichomes (cf. Figs.
751, 756).
Cells dividing lengthwise, i. e. parallel with the axis of trichomes, precede each
incidence of true branching. In some genera all cells in a trichome are able to divide
with more or less the same frequency (Nostocaceae). Although all vegetative cells
are primarily capable of division in a trichome, in several genera the most growth
is restricted to the apical or subapical regions of the trichomes and forms meristematic zones (Fig. 3). Cells in other parts of the trichome are in these cases mostly
inactive with regards to cell division. Meristematic zones rarely occur outside of
the apical/subapical region of the filaments, and indicate the functional diversity in
the multicellular cyanobacterial thallus. Subterminal meristematic zones are often
associated with more or less polarized trichomes, mainly in genera with morphologically modified trichome ends (Microchaetaceae, Rivulariaceae). However, they
also can occur in isopolar filaments with morphologically diversified trichome ends
(Scytonemataceae). In several forms terminal growth has been observed with intense division of terminal and subterminal cells. In other types, the ability to divide
is actually missing in terminal cells (which are usually in this case morphologically
different) and also in some prominent cells (e. g., heterocytes), or in cells forming
apical hairs. Contents of akinetes can start their intense and repeated division during the phase of their germination, where the enveloping thick cell wall layers split
or dissolve and the protoplast forms its own cell wall and intensely divides, forming a new trichome (germling).
True branching is present in several heterocytous families. It is initiated by a cell
division in a plane that is not perpendicular to the long axis of the trichome. One or
both of the cells resulting from this division change their polarity, divide repeatedly
perpendicularly or obliquely to the original trichome and form new branches physi-
Cells, Cell Division, Trichome Morphology 9
Fig. 4. Types of true branching: A-B – T-type in genera with uniseriate trichomes
(A – Hapalosiphon-type, B – Westiella-type); C-D – T-type in genera with multiseriate
trichomes (C – Fischerella-type, D – Stigonema-type); E-G – V-type (e. g., Hyphomorpha, Loriella, Mastigocoleopsis); H-K – reverse Y-type. Explanations: arrows –
direction of growth, H – initial stage of reverse Y-branching. (From © Anagnostidis &
Komárek 1990)
10 Phenotypic Characters of Heterocytous Cyanobacteria
Fig. 5. Development of true branching in uniseriate trichomes: A – T-type; B – Vtype; C-D – modifications of reverse Y-type. The dark cells are initiating (dividing with
changed polarity) for new true branches. (From © Golubić & al. 1996)
ologically connected with the mother trichome. True branching can occur in both,
uniseriate or multiseriate trichomes, in which sometimes several neighbouring cells
can grow parallel in a new lateral branch.
Several types of true branching were described (cf. Komárek & Anagnostidis 1989,
Anagnostidis & Komárek 1990). The most important review of true branchings in
cyanoprokaryotes was presented by Golubić & al. (1996). The main types, which
are characteristic for various clades of heterocytous cyanobacteria, are presented
in Figs. 4–5. The different types of true branching are characteristic for several
evolutionary lines (families) of heterocytous cyanobacteria, but some types occur
only sporadically in various groups.
True branching plays an important role in cyanobacterial taxonomy and was considered as the main character of the traditional order Stigonematales. True branching occurs really only in heterocytous cyanobacterial types, but it is not restricted to
one phylogenetic clade (Gugger & Hoffmann 2004). Special types of true branching are characteristic and dominate inside of various phylogenetic clusters, classified at the family level after molecular phylogeny-based revision. In the family
Cells, Cell Division, Trichome Morphology 11
Fig. 6. Comparison of isopolar (Scytonemataceae, Nostocaceae) and heteropolar
Microchaetaceae, Rivulariaceae) trichomes in main heterocytous families. Schemes of
trichomes, types of false branching and types of germinating hormogonia. (From ©
Komárek & Anagnostidis 1989)
Nostocaceae, true branching is absent, but exceptionally T-type of branching can
occur in cultures or as anomalies (Nostoc, Umezakia, Sphaerospermopsis). The reverse Y-type is characteristic for Symphyonemataceae, T-type for Hapalosiphonaceae, Nostochopsidaceae, Fischerellaceae and Stigonemataceae. These specific
types of branching are typical within families (or, at least, for a majority of genera
in these clusters), in spite of the fact that sometimes various types of true branching
are combined in some taxa (cf. Gugger & Hoffmann 2004). The correct recognition
of true branching is important and therefore the schemes of different modifications
of true branchings according to Golubić & al. (1996) are presented here (Fig. 5).
The polarity of trichomes (isopolar or heteropolar) is typically characteristic
within lineages (e. g., see differences between Scytonemataceae and Microchaetaceae) (Fig. 6). The polarized trichomes are usually characterized by the development of basal heterocytes and connected commonly with the development of
hormogonia and morphologically modified apical ends. Morphologically modified apical ends are distinct usually by narrowed segments of trichomes to a hair
with elongated hyaline cells, with widened cells, with shorter apical cells, deeper
12 Phenotypic Characters of Heterocytous Cyanobacteria
Fig. 7. Polarity of trichomes in nostocacean and rivulariacean/microchaetacean
types; H – position of heterocytes. (From © Komárek & Anagnostidis 1989)
Ultrastructure 13
constrictions between apical cells, widened thylakoids in cells similar to “vacuolisation”, etc. Polarity of trichomes and various morphological modifications are
often congruent with phylogenetic position of various taxa (at least they can be
considered as intergeneric features). Isopolar trichomes are characteristic, e. g.,
for Scytonemataceae and Nostocaceae, heteropolar trichomes are indicative of the
Rivulariaceae and Microchaetaceae (Fig. 7). However, currently some genera exist
in which both types are included, and their phylogenetic status is not clear yet. For
example, the genus Stigonema contains species with polarized thalli or isopolar
thalli.
The family Rivulariaceae is characterized by distinctly polarized trichomes typically ending in hairs composed of narrowed and elongated cells. However, hairs
can also develop in isopolar trichomes (Scytonemataceae, Symphyonemataceae).
The function of hairs is associated with phosphorus metabolism and was explained
particularly by Livingstone & Whitton (1982, 1983, 1984), Livingstone & al.
(1983) and Whitton (1987).
Ultrastructure
The fine structure of heterocytous cyanobacteria is more uniform than in coccoid
and simple trichal genera. However, numerous specific structures have been found
in this group and some modifications during their life cycles and in response to
environmental conditions (light intensity) have been described.
The cell walls have the same structure in all heterocytous taxa and the most prominent features in them are the microplasmodesms, connecting the cells in trichomes.
Study of strains in the genera Anabaena, Trichormus and Nostoc revealed the presence of distinct deep pits in the interior lamina of the plasma membrane in the septum region and corresponding protrusions on the protoplasmic surface (see, e. g.,
Giddings & Staehelin 1978). Microplasmodesms occur in all filamentous species
and in one cross wall from 100 to 250 irregularly distributed pores were found
(Fig. 8). A slightly different organization of cross-walls are septal areas in some
of the more complicated types (Stigonema), in which the pore channels (so called
“pit connections”) are visible between vegetative cells under the light microscope.
Butler & Allsopp (1972) reported that pit connections are traversed by central persistent remnants of the original cross-walls. Pores also can traverse the numerous
layers.
Thylakoids are usually dispersed in the whole cell volume in heterocytous genera
under stable conditions (Fig. 9A), but their abundance and particularly agglomeration in peripheral parts can be influenced by external factors, mainly light conditions (Wildon & Mercer 1963b, Peschek & Sleytr 1983) or salt concentration
(Blumwald & Tel-Or 1982). In the majority of heterocytous types a combination
of parietal, later irregularly disposed thylakoids near the cell wall was found (e. g.,
Peat & Potts 1987) as well as thylakoids spread over the cell volume (Pinevich
& Mamkaeva 1984), or more or less in combinations of partly longitudinally and
concentrically situated thylakoids (Wildon & Mercer 1963b, Peat & Whitton 1967,
Gantt & Conti 1969, Whitton 1972). Some authors also described change from the
parietal location of thylakoids in young cells (Miller & Lang 1971, Whitton 1972,
14 Phenotypic Characters of Heterocytous Cyanobacteria
Fig. 8. Microplasmodesmes between vegetative cells: A – Nodularia spumigena,
cross section (from © Šmarda & al. 1988); B – Tolypothrix tenuis (from © Metzner in
Geitler 1960)
Feldmann & Guglielmi 1973). On the other hand, Evans & al. (1976) did not find
distinct changes in ultrastructure during the life cycle in the taxa he studied. A characteristic whirled arrangement of thylakoids was described in Nostoc commune and
in several Fischerella and Stigonema strains (Butler & Allsopp 1972). In the more
complicated true branching cyanobacteria the thylakoids are still irregular, but often confined to the peripheral parts of the cell, although they can be distributed over
the whole cell volume (sometimes in less density; Peat & Whitton 1967, Thurston
& Ingram 1971, Nierzwicki & al. 1982, Couté 1982 and many others).
The fasciculation of thylakoids, their widening and organization of other organelles
in cells results often in the keritomy of cells, which is, however, not so distinct
and specific in heterocytous families. The wider variability in thylakoid arrangement and presence of other morphological characters decrease the importance of
keritomy for taxonomy in this group of cyanobacteria.
An interesting and not yet understood phenomenon in cellular ultrastructure is the
occurrence of intrathylakoidal spaces (widened thylakoids) (e. g., see in Fiore &
al. 2007) (Fig. 10). In cyanobacteria, typical vacuoles do not occur, but the phenomenon of “vacuolization” of cyanobacterial cells has sometimes been observ-
Ultrastructure 15
Fig. 9. Inner structure and patterns of thylakoid position within nostocacean cells:
A – Nodularia sphaerocarpa, without gas vesicles; B – Nodularia spumigena, with gas
vesicles (gv). (From © Šmarda & al. 1988)
able in the light microscope. Widened thylakoids occur in cyanobacteria from all
taxonomic groups, from the most simple up to complicated heterocytous types with
a diversified thallus, and their function as vacuoles is possible. They occur in morphologically complex forms, particularly in apical parts of trichomes, or, in contrast, in older, but intensely growing filaments. The function of this phenomenon is
not yet clear, it is very probably influenced by external factors, but their frequency
and locations in special parts of the thallus seems to be genus- or species-specific.
Aerotopes occur in the majority of planktic genera, sometimes obligately (several
Dolichospermum species) or facultatively (Anabaenopsis, Cuspidothrix, Cylindrospermopsis and others). The gas vesicles have in principle the same structure and
irregular location in cells as in coccoid and aheterocytous filamentous types (Fig.
9B). In the majority of genera the ability to form gas vesicles and aerotopes is
congruent with phylogeny and the presence of gas vesicles can be considered as a
generic marker in such cases. But there still exist a few genera in one phylogenetic
cluster, which contain forms with or without gas vesicles (planktic and benthic
types), e. g., Cronbergia or Nodularia. In the form and frequency of aerotopes, there
also probably exist specific differences and the obligate development of aerotopes
16 Phenotypic Characters of Heterocytous Cyanobacteria
A
B C
D
Fig. 10. Intrathylakoidal spaces in cells of Brasilonema bromeliae. (From © Fiore
& al. 2007)
in vegetative cells or in hormogonia is, at least, a good taxonomic intergeneric and
interspecific character.
Benthic or periphytic species with aerotope-producing hormogonia were first described by Canabaeus (1929), but they are now known in many genera from several families (Gloeotrichia, Tolypothrix, Trichormus, Hapalosiphon, Fischerella
and others). The importance of aerotope-producing hormogonia for distribution
in aquatic environments seems to be clear, but the induction of gas vesicles in response to NaCl concentration, decrease of concentration of nutrients, or changes in
light intensities has also been reported.
Numerous other structures have been recognized within cells of heterocytous
cyanobacteria, but their relationship to genotypic position is poorly known. The
phylogenetic relationship between Nostocaceae (Anabaena, Nostoc) and Rivulariaceae (Calothrix, Gloeotrichia) was supported by the presence in both of membrane delimited crystalline inclusions (Jensen 1985). For isolates from the family
Rivulariaceae, an additional structure was found and called “spherical bodies”, but
the function of these structures is unknown. Possible relationships between species
from different genera were proposed by Jensen (1985), but investigations of his
hypotheses have unfortunately not been pursued recent years.
The structure of the mostly polysaccharidic sheath enveloping the trichomes in all
filamentous cyanobacteria is widely variable (Fig. 11). For more on the modifications of these envelopes see information on p. 61 and 64.
Heterocytes and their Position in Trichomes
Heterocytes are morphologically and functionally distinct cells, which develop
facultatively in a monophyletic clade of the most complex (morphologically diversified) cyanobacteria (Figs. 6, 12). The different groups from this phylogenetic
cluster have been traditionally classified as the orders Scytonematales, Nostocales
and Stigonematales. Heterocytes develop in intercalary position and/or terminally
(or in bases of polarized trichomes) from vegetative cells and occur obligately in
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