as tools in studying the biosynthesis of cellulose,
nature's most abundant macromolecule
Malcolm Brown, Jr.
Department of Botany
The University of Texas at Austin
Austin, Texas 78712
Experimental Phycology. Cell Walls and Surfaces, Reproduction, Photosynthesis. 1990 (pp 20-39)
Ed. W. Wiessner, D.G. Robinson, and R. C. Starr
Berlin Heidelberg New York
London Paris Tokyo
Hong Kong Barcelona
The most dominant polysaccharide
of the cell wall is
cellulose. The universal distribution of this natural polymer
among prokaryotic and eukaryotic organisms attests to its
ancient evolutionary history. Not only is cellulose found
among photosynthetic and protistan cells, it is present in
animals such as the Ascidians (Wardrop, 1970). Furthermore,
levels of elevated cellulose synthesis have been suggested in
humans with the disease scleroderma (Hall, et al, 1960).
The algae have been prominent organisms
of study among
eukaryotic organisms because of their great diversity of
structure and cellular organization. Chloroplast morphology
(Gibbs, 1981), organization of the mitotic apparatus (Pickett-
Heaps, 1972), cell wall structure and composition (Preston,
1974), flagellar apparatus (Stewart and Mattox, 1978), and
reproduction have provided a wealth of information on algal
phylogeny (Stewart and Mattox, 1982); however, very few
studies have concentrated on evolutionary and phylogenetic
aspects of cell walls, let alone cellulose, mainly because
the cellulose synthases had never been observed or isolated.
In 1976, the first
successful application of freeze
fracture demonstrated the structure of a cellulose synthase
complex in Oocystis apiculata (Brown and Montezinos, 1976).
These membrane associated structures, called terminal
synthesizing complexes (=TCs), were found at the growing tip
of microfibril impressions on the E-fracture face of the
plasma membrane. Earlier, Roelofsen (1958) had predicted that
an organized terminal enzyme complex would be found; however,
the shape and geometry could not be predicted at that time.
In 1964, Preston proposed the ordered
for the cellulose synthase complex. This study was based on
observations of remnants of organized particle subunits
associated with the innermost wall of Chaetomorpha. During
this time, the freeze fracture technique was becoming widely
used, and organized particle complexes were found in the
plasma membranes, particularly abundant in yeasts (Moor and
Muhlethaler, 1963). Thus, a logical extension of the
possibility of such an organization could be made for the
cellulose synthesizing complex. Interestingly, TCs were not
observed in cells which had been chemically fixed or treated
with glycerol or cryoprotectants. The breakthrough in finding
TCs came when Brown and Montezinos demonstrated that rapid
direct freezing of living cells yielded organized particle
structures associated with the tips of microfibrils.
Since 1976, TCs have been found in
more than 14 algal
genera, and presently, a distinct pattern of TC structure is
beginning to emerge which provides some insight into the
substantial diversity of cellulose microfibril synthesis
among the algae. In this presentation, the fundamental TC
diversity among the algae will be described. Because TC
variation is the greatest among the algae, it also provides
hints at the relationship between TC organization and
microfibril shape, molecular weight of the cellulose, and
crystallization. Phylogenetic relationships based on TC
structure can be correlated with other structural and
biochemical evidence. This presentation will conclude with a
proposed evolutionary history of cellulose biogenesis.
TERMINAL COMPLEX DIVERSITY
So far, only two basic
forms of TCs have been found
among eukaryotic cells. The linear TC was first discovered in
Oocystis and is present among most members of the Ulvophyceae
(Hotchkiss and Brown, 1989) (Fig 1). The rosette TC was
reported simultaneously by Mueller and Brown (1980) and
Giddings, et a], (1980). Earlier, Mueller, et al (1976) had
observed a globular component of the TC on the E-fracture
face of the plasma membrane in corn roots. Subsequent
examination of the P-fracture face revealed a rosette of 6
symmetrically organized particle subunits (Fig 2).
Unlike that in the corn root, the
rosette TC found in
Micrasterias frequently is organized in ordered arrays,
especially during secondary wall formation (Giddings, et al,
1980). Furthermore, the rosette subunits have been shown to
span both layers of the bimolecular leaflet. Since these
first reports, rosette TC's have been found in a variety of
organisms, ranging from the land plants to Chara (McLean and
Juniper, 1986) and Nitella (Hotchkiss and Brown, 1987).
For a more detailed elaboration of
the distribution of
TC's among eukaryotic cells, consult the report of Brown
(1985). Since this publication, TCs have been found in other
organisms and will briefly described. In 1987, Hotchkiss and
Brown described a solitary rosette TC in Nitella translucens
(Hotchkiss and Brown, 1987). This TC is virtually
indistinguishable from that of land plants, in addition, a
solitary- rosette TC has been observed in Chara (McLean and
Only in the Zygnematales has an ordered
of TC's been found, and among one member, Mougeotia, the TCs
are exclusively solitary (Hotchkiss et al 1989 ). Thus, the
consolidation of rosette TCs appears to have been a more
recent event (Hotchkiss and Brown, 1989a). When wall
composition is taken into consideration, the evidence
strongly supports that the Charophyceae is the phylogenetic
line which may have given rise to the vascular plants.
Another interesting and different
TC structure recently
was found in the xanthophycean genus, Vaucheria (Mizuta et
al, 1989). Overall, the TC is linear, but the subunit
arrangement within the TC is in the form of unique diagonal
rows (Fig 3).
THE EVOLUTION OF THE TC AND CELLULOSE BIOGENESIS
Based on TC ultrastructure and cellulose
it is possible to construct a phylogenetic pathway for
cellulose biogenesis (Fig 4). Although somewhat premature,
this treatment gives several important and interesting clues
to the subject of eukaryotic cellular evolution. Clearly, the
algae as a group have been pivotal in the diversification of
cellulose microfibril assembly as exemplified by the
diversity of TC and microfibril morphology.
The evolution of cellulose among
prokaryotic cells will
first be considered. The fact that cellulose assembly occurs
among two widely divergent prokaryotic groups suggests that
this process must have been an ancient one. The
investigations of Woese have shed much light on bacterial
evolution. Using homologous sequences in rRNA, it has been
possible to unambiguously examine and measure phylogenetic
relationships among the bacteria (Woese, 1987).
The genus, Sarcina
is a gram + bacterium and is
considered primitive among the eubacteria. Sarcina also is an
obligate anaerobe. Cellulose synthesis in Sarcina was first
described by Canale-Parola et al (1961). We have also studied
cellulose synthesis in Sarcina (Roberts and Brown,
unpublished data) and have come to the conclusion supporting
Canale-Parola et al that only the cellulose II polymorph is
synthesized. The exact site of cellulose synthesis is
unknown; however, membrane fractions of Sarcina can
synthesize cellulose II in vitro (Lin, Roberts, and Brown,
Among the purple
bacteria, only the cellulose I
polymorph is synthesized (one exception is a mutation in
Acetobacter giving rise to cellulose II synthesis, see
Roberts et al, 1989). The site of cellulose microfibril
synthesis is a linear row of particles parallel to the
longitudinal axis of the cell (Brown et al, 1976). On the
surface of the LPS layer of the cell envelope is a pore
complex through which fibrils are extruded. The enzyme
complex is located in the cytoplasmic membrane (Bureau and
Brown, 1987).- Groups of three or more particles are required
to assemble subfibrils which consolidate to form a
microfibril tangential to the cell surface (Haigler et al,
1980). Microfibrils unite to form bundles which, in turn,
group to assemble ribbons. The ribbons are visible with
darkfield microscopy, and the progress of cellulose synthesis
can be directly monitored using time lapse video microscopy
(Brown and Santos, unpublished observations; Brown and
Colpitts, 1978; Lin and Brown, 1989).
In Rhizobium and Agrobacterium,
the sites of cellulose
assembly are similar; however, fewer microfibrils
consolidate. Only a floe of cellulose is produced, while in
Acetobacter, a thick leathery membrane or pellicle is
synthesized. The function of cellulose biosynthesis in
-Acetobacter is_ unknown. Acetobacter xylinum is an obligate
aerobe. Therefore the buoyancy of its cellulose could provide
an aerobic environment for cells active in cellulose
synthesis (Schramm and Hestrin, 1954). Why Acetobacter would
divert large pools of metabolic substrate into cellulose is
unknown; however, cellulose could serve as a reserve pool for
metabolism. Unfortunately, extensive cellulase activity has
not been found; yet, degradation of non-crystalline
carboxymethylcellulose can occur (Brown and White,
investigations of cellulose
biogenesis in Acetobacter have yielded perhaps the most
extensive evidence for the molecular mechanisms of cellulose
assembly. Cellulose has now been synthesized in vitro
(Glaser, 1958); a specific activator for cellulose synthesis
has been found (Ross et al, 1985), the in vitro product
characterized morphologically (Lin et al, 1985), the in vitro
crystalline polymorph deduced (Bureau and Brown, 1987), the
cellular site of the synthase localized (Bureau and Brown,
1987), the cellulose synthase purified (Lin and Brown, 1989,),
and gene cloning for the purified enzyme initiated (Saxena
and Brown, 1989).
Cellulose synthesis among the blue
green algae has been
mentioned only once in the literature, and conclusive
evidence for this is lacking (Frey-Wyssling, 1976). According
to Woese (1987), the cyanobacteria emerged from the distance
matrix phylogenetic tree of the eubacteria almost from the
same region as the gram + bacteria and also close to the
purple bacteria. Thus, it is clear that cellulose biogenesis
must have been an ancient process during the evolution of
life on earth.
With the accumulating evidence of
among prokaryotes, the evolution of cellulose among this
group can now be addressed. The cellulose II polymorph
appears to be primitive. This polymorph is the more
thermodynamically stable form with an additional inter-chain
H-bond formed per glucose residue. Cellulose II can form
spontaneously from solution when cellulose is solubilized by
such agents as DMSO/paraformaldehyde or cupraammonium
reagents (Blackwell et al, 1986). On the other hand,
cellulose I is a metastable polymorph, presumably
assembled only by living organisms. Therefore, cellulose I is
more advanced, requiring additional mechanisms for chain
orientation and positioning to achieve the metastable state.
The first cellulose
producer probably had its glucan
synthase randomly organized in association with the membrane
(Fig 5). Under these primitive conditions, only cellulose II
could bioynthesized in vivo. Thus, in Sarcina, glucan chains
appear to be randomly positioned over the cell surface in an
amorphous array. Sarcina is an excellent example of an extant
organism which lacks mechanisms to consolidate and organize
the glucan synthase complex to induce ordered microfibril
assembly and aggregation into bundles and ribbons of
cellulose 1. On the other hand, the purple bacteria evolved
the mechanisms to order glucan chains into various
conformations leading to a diversity of cellulose I
microfibril assembly. Because of abundant evidence suggesting
that the purple bacteria are more advanced (Woese, 1987), it
follows that cellulose I assembly is more advanced. A logical
extension of this evolutionary advancement is to consider the
evolution of cellulose among the eukaryotes. Did these cells
obtain genes for cellulose synthesis from the eubacteria? If
so, what are the likely candidates? It is obvious that if the
mitochondria of eukaryotes came from the purple bacteria, did
they also transfer the genes for organized cellulose I
synthesis? This is an intriguing question, one which must
await cloning and sequencing of the genes for the cellulose
We shall now consider one of the
greatest mysteries in
biology- the origin of cellulose synthesis among eukaryotic
cells. The possibility that the genes for cellulose synthesis
may have come from the purple bacteria has been alluded to.
What was the first eukaryotic organism to have received the
cellulose synthase gene? An examination of phylogenetic trees
indicates that among the extant primitive eukaryotes,
cellulose is found among one group, namely, the cellular
slime molds. Cellulose I of low crystallinity has been found
in Dictyostelium (Roberts and Brown, unpublished data).
Because Dictyostelium is non-photosynthetic, it seems highly
unlikely that it could have received the genes for cellulose
synthesis from a photosynthetic prokaryotic progenitor. It
seems attractive, therefore, that the purple bacteria may
have donated these complexes.
Dictyostelium TCs are unlike any
so far found among
eukaryotic cells. They appear to consist of linear arrays of
single particles (Fig. 4' (Mizuta and Brown, unpublished
results). These arrays are somewhat similar to those found in
Acetobacter. Thus, among eukaryotic organisms, the linear
arrangement of single rows of particle subunits (arrows) in
Dictyostelium appears to be primitive. This is also supported
by the low crystallinity of cellulose I from this organism.
Certain fungi, among
them, the Oomycetes, synthesize
cellulose. Yet, nothing is known of TC structure among the
fungi. This is a major research area which needs immediate
attention. One could predict, however, that if Vaucheria is
closely related to Saprolegnia, the unique linear TC with
diagonal rows (Mizuta and Brown, 1989) might be found in the
Why many of the fungi opted for chitin
as the major
wall polymer is an interesting sidelight to the question of
the evolution of cellulose synthesis. Some of the fungi are
almost as primitive as Dictyostelium, yet there is scant
knowledge of chitin synthesis among primitive eukaryotes, let
alone the eubacteria and archaebacteria. Perhaps nutrition
may have played a role in the more efficient utilization of
strong polymers. Since chitin walled organisms may have
required more nitrogen, the energy budget would be greater.
Thus, to synthesize a polymer of cellulose would represent a
selective advantage from a nutritional point of view
(Duchesne and Larson, 1989).
EVOLUTION OF CELLULOSE SYNTHESIS AMONG PHOTOSYNTHETIC
At this junction, the
algae certainly have played a
diversified role, for it is here that the greatest variety of
TCs and cellulose structure is found among the algae (Fig 6).
Gunderson et al, 1987) have suggested on the basis of 18S
rRNA sequences that a cellulose producing oomycete, Achlya
bisexual is, is closely related to Ochromonas danica, a chitin
producer. Perhaps the fungi and chromophytes appeared at
roughly the same time.
The recent studies of Pearasso
et al, 1989) have shed
some light on the origin of the algae. On the basis of 28S
cytoplasmic rRNA homology, they found that three distinct
groups emerged late among eukaryotes: rhodophytes,
chromophytes, and chlorophytes. A late occurrence of
eukaryotic photosynthetic symbiosis was implied. The
conserved rosette/linear TCs among the algae suggests that
the synthase may have come from the more primitive fungi or
Dictyostelium, rather than through the chloroplast. Again,
this implies that even earlier, the ancient eukaryotic
mitochondrion may have contained the genes for cellulose
Could the cellulose synthase of the
Rhodophyta have come
from the cyanobacteria? This question cannot be answered
until we have more data on the presence and physical
characteristics of cellulose among the cyanobacteria. If only
cellulose II is present among the cyanobacteria, it would be
difficult to imagine an independent evolutionary event to
organize the TC to allow it to produce cellulose I which is
found among the Rhodophyta. If, however, Nostoc is found to
produce cellulose I in vivo, the hypothesis that the
cyanobacteria could have been the progenitors of the
Rhodophyta, would be strengthened. It should be apparent that
these questions cannot really be answered, let alone
seriously considered, until we have sequence information on
the cellulose synthase; yet these questions do need to be
placed before the scientific community now so that the
blueprint for solving this great mystery can be expedited.
The origin of cellulose synthesis
among the major algal
groups is still a major mystery. Consider that cellulose is
known among the Pyrrophyta, the Chrysophycease, the
Xanthophyceae, the Phaeophyta, and the Chlorophyta (Fig 6).
Did each of these major groups receive a cellulose synthase
independently, possibly from pro-chloroplast capture? The
diversity of TC structure among these groups might suggest
multiple independent captures, yet only the purple bacteria
are known to synthesize cellulose I, the same polymorph found
among the great diversity of algae (with the exception of
Halicystis, Sisson, 1938; Roberts and Brown, 1989,
unpublished data). This argues in favor of a single capture
of the cellulose synthase very early in eukaryotic evolution,
possibly through the purple bacteria donation of the pro-
mitochondrial apparatus. This implies that the organizational
machinery for glucan chain assembly into the cellulose I
polymorph may have also been introduced early through
transfer to an ancient eukaryotic progenitor. Then,
Dictyostelium may be an example of one of the most ancient
surviving groups which received the cellulose synthase from a
prokaryotic progenitor. These are provocative questions, but
ones which cannot be answered with certainty at present.
Possible evolutionary pathways of
biogenesis, showing the relationship of the algae to early
Cellulose synthase is an ancient
molecule as evidenced
by its ubiquity among prokaryotic and eukaryotic organisms. It
therefore must have served an important early function in the
origin of life on earth. The most advanced eukaryotic land
plants have the rosette cellulose synthase TC. Advanced
members of the Charophyta have the rosette TC, an so do
members of the Zygnemetales. At present, all pieces to the
puzzle are not in place. Critically important algae need to
be investigated for their TC structure to provide more direct
confirming data for the rosette TC in land plant evolution.
These include Coleochaetae, members of the Trentepholiales
(Cephaleuros), the Klebsormidiales (Klebshormidium), the
Chlorokybales (Chlorokybus), and other members of the
Zygnematales ( Zygnema, Netrium) .
The concept of
symbiotic capture of the cellulose
synthase in eukaryotic cells needs more study (Fig 7). Did
the cellulose synthase come from a mitochondrial progenitor
(through the purple bacteria)? Did it originate through a
chloroplast progenitor (from the cyanobacteria, pro-
chlorophyta, or pro-chromophyta)? Did the cellulose synthase
transfer directly from the prokaryote chromosome or plasmid?
Perhaps one or more symbiotic captures occurred, giving rise
the the diversity of TC morphology and microfibril diversity.
The known diversity of cellulose
degree of polymerization, and crystallinity, suggests that
secondary modifications to the primary glucan synthase must
have occurred. Perhaps even the regulation of cellulose
synthase activity has been modified, although cellulose
synthase activity appears largely constitutive. The diversity
of fibrillar polymers other than cellulose among the algae
supports an extremely diverse evolution in cell wall
structure, possibly reflecting the wide range of environments
Algae have served as
excellent model systems in the
quest for understanding cellulose biogenesis. Not only do the
algae synthesize diverse forms off cellulose, they offer an
uncompromising approach for cytological observation, coupled
with a potential for isolation, cloning, and sequencing of
the genes involved in cellulose biogenesis. The coming decade
will see great advances in cellulose biogenesis research.
Appreciation is expressed
to Richard Santos for his
unfailing loyalty and support throughout the past 19 years.
Also, my former and present graduate students, post-doctoral
fellows, and visitors to the lab deserve recognition for
their contributions to this research. I thank Inger Johansen
for preparing this manuscript. This research was supported by
the National Science Foundation, The Johnson & Johnson
Centennial Chair Endowment, and funds from the University of
Texas at Austin.
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Cell Walls and Surfaces
W. Wiessner, D. G. Robinson
and R. C. Starr
With 91 Figures
Berlin Heidelberg NewYorl
London Paris Tokyo
Hong Kong Barcelona
Professor Dr. WOLFGANG WIESSNER
Professor DAVID G. ROBINSON
Pflanzenphysiologisches Institut der Universitat
Untere Karspiile 2
3400 Gottingen, FRG
Professor RICHARD C. STARR, Ph. D.
The University of Texas at Austin
Austin, TX 78712, USA
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