The Blue-green Algae

466 Pages·1973·17.75 MB·English

by  G.Fogg (Auth.)

Blue-green algae from a wet rock face, Salen, Isle of Mull, Scotland;
Petalonema alatum Berk, (filamentous with complex sheath), Gloeocapsa
alpina Nag. emend. Brand (unicellular, violet sheath) and Gloeocapsa
montana Kutz. (unicellular, colourless sheath), x 400. E. F. Wilkinson,
after a water colour drawing by G. E. Fogg.
THE
BLUE-GREEN
ALGAE
G. E. FOGG, W. D. P. STEWART
P. FAY and A. E. WALSBY
1973
Academic Press - London and New York
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Copyright © 1973 by
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Library of Congress Catalog Card Number: 72-12269
ISBN: 0-12-261650-2
PRINTED IN GREAT BRITAIN BY
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Preface
The blue-green algae, for a long time a disregarded group of micro­
organisms, are now a fashionable subject for research. The possible reasons
for this are various. One may be that current speculations about the origin
and early evolution of life have reminded biologists that this is a group of
undoubted antiquity. It has biochemical characteristics, on the one hand,
which may be related to an existence on the primitive Earth and, on
the other hand, it shows possible links with the green plants which are
dominant today. Another reason may be that the electron microscope has
revealed features of fine structure which confirm the long suspected kinship
of these organisms with the bacteria. Mounting evidence that blue-green
algae play an important, if unobtrusive, part in maintaining soil fertility
and the often all too obvious fact that they are a nuisance in freshwater
have also made their study of some economic importance.
For the four authors of this book this upsurge of interest has been
exhilarating, as ways of solving apparently insoluble problems have
presented themselves, facts have fallen into place and new, intriguing,
questions have arisen. Nevertheless they are already conscious of the
increasing mass of specialist literature and feel that now, before it becomes
overwhelming, is the time to attempt the assembly of a unified picture of
blue-green algae as living organisms. They hope that the result will be of
use to students and research workers in various branches of botany,
microbiology and biochemistry. On a more personal level this book is a
tangible reminder of a most happy period of collaboration in the Depart­
ment of Botany at Westfield College, University of London.
The authors* thanks are due to many people who have generously given
their help in this enterprise. Successive versions of the text have been
typed by Mrs. N. Last, Miss Marianne Joyce and Mrs. B. Cunningham.
Dr. Hilda M. Lund has given us considerable help with the chapter on
pathogens. We also thank Mr. Ray Mitchell and Miss Gail Alexander for
help with photographs and figures. The names of those who have allowed
the use of copyright illustrative material, thereby greatly enhancing the
usefulness and appearance of the book, are too numerous to mention here
but will be found in the appropriate places in the text. Lastly, the patience
v
and forbearance of the publishers in the face of repeated delays on the
part of the authors must be acknowledged.
February y 1973
G. E. FOGG W. D. P. STEWART
Department of Marine Biology, Department of Biological Sciences,
University College of North Wales, The University,
Marine Science Laboratories, Dundee DD1 4HN,
Menai Bridge, Anglesey, Scotland.
North Wales.
P. FAY A. E. WALSBY
Department of Botany, Department of Botany,
Westfield College University of California,
(University of London), Berkeley, California 94720,
London N.W.3, U.S.A.
England.
VI
Chapter 1
Introduction
The micro-organisms known as blue-green algae form an unusually
well-defined group. Blue-green algae are not always blue-green in colour
but after a little experience one can recognize them instantly under the
microscope because of the characteristically homogeneous appearance
which the absence of membrane-bound organdíes, such as nuclei and
chloroplasts, gives to their protoplasm. In distinguishing the smaller
species from bacteria, which also lack such organdíes, there may be some
difficulty. However, the blue-green algae usually contain the pigments
chlorophyll a and biliproteins, by means of which they carry out photo­
synthesis with the production of oxygen, whereas bacteria, if photosyn-
thetic, have other pigments and do not produce oxygen. Furthermore,
blue-green algae, although they may show a characteristic gliding move­
ment, never possess flagella as means of locomotion as some bacteria do.
Only with some colourless species which have close morphological resem­
blances to blue-green algae but lack their photosynthetic apparatus, may
there be uncertainty about taxonomic position.
Mentions of remarkable growths in fresh water, which we now know to
have been planktonic blue-green algae, are found in early records such as
those which Giraldus Cambrensis wrote in 1188. Shakespeare assumed that
his audiences were familiar with such manifestations when he put into the
mouth of Gratiano in the Merchant of Venice the words "There are a sort
of men whose visages do cream and mantle like a standing pond". However,
the first scientific descriptions of particular kinds of blue-green algae did
not appear until the early nineteenth century. Roth between 1797 and 1806,
distinguished the genus Rivularia and Vaucher in 1803 described Oscilla-
tona and Nostoc. Vaucher placed these blue-green algae in the animal
kingdom but nevertheless their subsequent study was undertaken mainly
by botanists. Harvey (1846) put the blue-green algae together with green
algae in a group Chlorospermae but as biologists learnt more about the
internal structure of cells and the significance of the photosynthetic pig­
ments it was realized that there are important differences between the two
kinds of organism. The blue-green algae were segregated as a distinct group,
2BGA 1
2 THE BLUE-GREEN ALGAE
the Myxophyceae, by Stitzenberger in 1860. This name has priority but
has not been universally accepted because it is liable to be confused with
Myxophyta, which denotes the slime moulds. The name Cyanophyceae,
introduced by Sachs in 1874, has usually been preferred as it conforms
with the principle of naming algal groups according to their characteristic
colours. In the present day classification of the algae, the basic pattern of
which was crystallized by Pascher in 1914, the group is given the rank of a
division of the plant kingdom under the name Cyanophyta, a term intro­
duced by Smith in 1938 (a fuller account of the history of phycology is
given by Smith, 1951).
In gross morphology and nutrition the blue-green algae have many
features in common with the other algal groups and it is therefore con­
venient to deal with them as algae for many purposes. However, as long ago
as 1853, Cohn drew attention to the similarities between blue-green algae
and bacteria and in 1871/2 put them together in a division Schizophyta,
giving the name Schizophyceae to the former and Schizomycetes to the
latter. The name Schizophyceae has not been widely used but the affinity
of the blue-green algae and bacteria has been substantiated by modern
work. Indeed, some authorities (Stanier et aln 1971) categorically state that
blue-green algae are bacteria. This recognition of the affinities of the two
groups has grown largely out of studies of fine structure. Cells of blue-green
algae are small, generally being only a few micrometres in diameter,
about a tenth of that of an average cell of a higher plant or animal. The
details of subcellular structure are often near the limits of resolution of the
light microscope. Although it is remarkable how much information was
collected by the early workers, real progress scarcely began until, somewhat
tardily, the electron microscope was used. Although much remains to be
learnt it has become quite clear that the blue-green algae share with the
bacteria a type of cellular organization known as prokaryotic. This stands in
sharp contrast to the eukaryotic type of cell, with membrane-enclosed
nucleus, shown by all other types of organism. Also certain bacteria and
blue-green algae produce a unique type of gas-containing subcellular
structure, the gas vesicle, which confers buoyancy on the algae. Classifica­
tion of the blue-green algae alongside the bacteria in the kingdom Pro­
karyota is therefore a truer representation of their phylogenetic position
than classification with the other algal groups, which together with higher
plants and animals constitute the kingdom Eukaryota.
The interest of the prokaryotic state to the biologist scarcely needs
emphasis. The basic chemical mechanisms on which life is based are
generally similar in the Prokaryota and Eukaryota but they are carried out
in somewhat different structures in the two kingdoms. The sequence of
reactions in aerobic respiration, for example, is generally similar although
1. INTRODUCTION 3
in Eukaryota the enzymes concerned are contained in specific membrane-
bounded organdíes, the mitochondria, whereas in Prokaryota they are
associated with simpler membranous structures. Comparison of the
molecular architecture and efficiency of these two types of structure is of
obvious interest. The relatively simple cell structure of the Prokaryota
gives an impression of being primitive and its antiquity is indicated both
by the evidence of fossils and biochemical considerations. Study of the
Prokaryota may thus shed light on the origin of life on the one hand and the
evolution of the Eukaryota on the other. Beyond this, the small size, lack
of differentiation, ease of culture and handling, and rapid growth of certain
Prokaryota has made them excellent experimental material for investiga­
tion of a great variety of general biological problems. One may call to mind
here the enrichment of biochemistry by study of the tremendous variety of
metabolic processes exhibited by the bacteria and the massive contribution
which research utilizing Escherichia coli has made to molecular biology. In
all this, however, work with blue-green algae has so far played little part.
There are various reasons for this. Blue-green algae are often difficult to
isolate and grow in culture and a belief, largely unfounded, that they grow
extremely slowly was current at one time. Few of them are even indirectly
pathogenic and, until recently, none has been considered of great impor­
tance either as being a nuisance or being useful. Thus, there has not been
the urgency and economic incentive in their investigation that there has
been with certain bacteria. Nevertheless it is important that the kind of
investigations that have been carried out with bacteria should also be made
with blue-green algae. Even if it were to turn out that their biochemical and
genetical mechanisms closely parallel those of bacteria, a point of general
biological importance would have been established, but there are certainly
interesting differences that should be investigated. In some respects blue-
green algae appear to possess different biochemical machinery to the
bacteria for there are indications that they lack some of the mechanisms of
control of enzyme synthesis possessed by bacteria. The photosynthetic
mechanism of blue-green algae differs distinctly from that of bacteria
both in the chemical nature of the pigments carrying out the photochemical
reactions and in the involvement of oxygen liberation from water. Here, in
fact, we have the type of photosynthetic machinery characteristic of the
higher plants present in prokaryotic cells.
Another point is that the greater extent of cellular differentiation and
morphological elaboration exhibited by the blue-green algae offers the
possibility of extending molecular biology into fields which could not be
tackled using bacteria as experimental material. Two kinds of differentiated
cell are produced by blue-green algae : spores (or akinetes) and heterocysts.
The former, although different from bacterial spores in their method of
4 THE BLUE-GREEN ALGAE
formation and in appearance, have, like them, the function of tiding the
species over periods of adverse conditions. The function of heterocysts,
empty-looking thick-walled cells, has for long baffled phycologists and
earned these structures the title of "botanical enigmas'' (Fritsch, 1951).
The recent discovery of the specialized biochemical activities of the
heterocyst indicates their probable function as that of nitrogen fixation but
they still present many problems. Whatever their significance, their
regular positioning in the filament seems to present a simple linear morpho-
genetic situation particularly suitable for experimental investigation.
The evolutionary potentialities of the prokaryotic cell are evidently
strictly limited as compared with those of eukaryotes. This perhaps depends
both on a limited capacity for genetic recombination and on the restrictions
on specialization and organization of cells imposed by the non-compart­
mentalized type of cell structure. The blue-green algae include unicellular,
colonial and filamentous forms and the most advanced type of morpholo­
gical structure attained is the multiseriate branched filament. Within this
range there has been evolution parallel to that in the eukaryotic algal classes.
The broad classification of these forms into the five orders Chroococcales,
Chamaesiphonales, Pleurocapsales, Nostocales and Stigonematales sug­
gested by Fritsch (1942) is generally accepted although it is becoming
apparent that at least the first of these is polyphyletic (Kenyon and
Stanier, 1970). Stanier et al, (1971) have established on the basis of cell
physiology, fatty acid composition and DNA base composition, that
several distinct and widely separated groups can be discerned in the
Chroococcales. They have demonstrated that it is possible to make such
taxonomic distinctions only by investigations with organisms in pure
culture, a statement which will no doubt prove to be also true of the other
major groups of blue-green algae. It is not proposed to discuss the taxonomy
of the blue-green algae in any detail in this book but the comment must be
made that at the levels of genus and species the situation at present is
chaotic. In taxonomic works such as those of Geitler (1932) and Desika-
chary (1959) distinction between species is frequently made on the basis
of characters, such as trichome diameter and the form of the sheath, that
may vary according to environmental conditions. Drouet has made a
laudable attempt to reduce the number of species and systematize their
classification into genera but has taken little account of experimental
studies; perhaps, in reducing more than 1000 specific and subspecific taxa
of the coccoid families to 30 (Drouet and Daily, 1956), he has gone too far
in the direction of simplification. The taxonomic treatment of the Chro­
ococcales by Stanier et al. (1971) provides a model for work on other orders
of blue-green algae. No major taxonomic treatment has yet taken account
of the fact that the presence or absence of heterocysts, which has often
1. INTRODUCTION 5
been used as an important diagnostic feature in filamentous forms,
depends on the concentration of combined nitrogen in the medium as well
as on the genotype and in turn has far-reaching repercussions on the
general morphology of the alga. Perhaps the numerical taxonomy approach
advocated by Whitton (1969) will ultimately prove to be one solution to
these various problems. Meanwhile the nomenclature used by the indivi­
dual authors whose papers are quoted will be followed in this book.
The ability of the blue-green algae to fix the free nitrogen of the atmo­
sphere has attracted the attention of ecologists, physiologists and bio­
chemists. At present it appears that this remarkable biochemical process is
confined to Prokaryota. Towards the end of the nineteenth century, at a
time when identification of the principal nitrogen-fixing agents was
beginning, some microbiologists were convinced that blue-green algae were
particularly important. Frank (1889) found nitrogen fixation associated
with the growth of these algae on soil and Prantl in the same year reported
on nitrogen fixation in cultures of Nostoc, but their experiments provided
no proof that these, and not accompanying fungi or bacteria, were the
organisms responsible. Three years later Schloesing and Laurent (1892)
reported that two Nostoc species fixed nitrogen in impure culture whereas
another blue-green alga, Microcoleus vaginatus did not. Beijerinck (1901)
obtained copious growth of certain species of blue-green algae in media
containing no source of combined nitrogen but, being unsuccessful in
isolating the algae in pure culture, was unable to substantiate his conviction
that they fixed free nitrogen. It was incidentally in the course of this work
that he characterized the well known nitrogen-fixing bacterial genus
Azotobacter. Axenic cultures of blue-green algae were eventually obtained
by Pringsheim (1914) but he and his pupils Glade (1914) and Maertens
(1914) failed to find evidence of nitrogen fixation by the species isolated.
This finding is somewhat inexplicable since some of the species belonged
to genera which we now know to be characterized by this property. It led
to the belief that blue-green algae are not themselves capable of nitrogen
fixation and that their ability to grow in media deficient in combined
nitrogen depended on symbiotic association with nitrogen-fixing bacteria
(see, for example, Jones, 1930). Conclusive proof that some species of
blue-green algae are themselves able to fix nitrogen was provided by
Drewes in 1928 but by then Azotobacter, Clostridium and the legume
nodule symbiotic association had become established as the "classical"
nitrogen-fixing systems and interest of biochemists and agriculturalists in
the algae was slight. It was not realized that in combining capacities for
photosynthesis, nitrogen fixation and growth under aerobic conditions the
blue-green algae have a unique potential for contributing to productivity
in a variety of agricultural and ecological situations and for many years