Bacterial Cells

Terry J Beveridge, University of Guelph, Guelph, Ontario, Canada

Bacteria are prokaryotes and therefore have a simple cell structure. There is no nucleus and genetic material is free within the cytoplasm. The two fundamental types of bacteria Gram-positive and Gram-negative have different cell wall structures.

Introductory article
Article Contents
. Introduction . General Description of Cell Structure . Specialized Internal Structures . Shape and Form . Biofilms

Introduction
Bacteria (previously termed eubacteria) are a lineage of prokaryotic cells that split o from the ancestral lineage relatively early in the evolution of life. After this time, two prokaryote domains existed, the Bacteria and the Archaea. Eukaryotic life emerged at a later date from the archaeal lineage. The general structural imprint for bacterial life seems to have been well established during the development of the ancestral lineage since the fossilized remains (microfossils) of such ancestors have been found preserved in organic-rich cherts and shales dating back to about 3000 3600 million years ago. These remarkable imprints of simple lifeforms do not reveal much structural detail (Figure 1), but they do demonstrate that prokaryotic cells (at that early time) were similar in shape and size to presentday bacteria. The common features that are retained today are: (1) small size, (2) simple cellular organization, (3) robust cell envelopes and (4) binary ssion for reproduction. Clearly, this is a design strategy that has been highly successful for the last 3600 million years and it has been malleable enough to change with (or withstand) the stressful inuences (some of which have been globally catastrophic for long time periods) on bacteria over eons.

. Enveloping Structures . Gram-staining Properties . Motility Structures . Specialized Structures for Survival . Concluding Remarks

General Description of Cell Structure

Bacteria are small ( $ 1.52.5 mm3) cells of relatively simple construction (Figure 2) as compared to eukaryotic cells. Most have a single, circular chromosome that entwines itself throughout the cytoplasmic matrix. (Recent studies suggest that some bacteria, such as Borrelia and Agrobacterium have a linear chromosome and that others, such as Rhodobacter, Leptothrix, Brucella, Burkholderia and Rhizobium, have multiple nuclear elements some of which are too small to be considered true chromosomes.) Unlike eukaryotic cells, bacteria do not compartmentalize their cytoplasm into separate functional organelles. For this reason, the bacterial chromosome is not bound by a nuclear envelope and the cytoplasmic space it occupies is referred to as the nucleoid (Figure 2). As the cells grow in size, the chromosome is constantly replicating so that, by the time of division, each daughter cell obtains an equal

chromosomal complement. Sometimes, under optimal growth conditions, bacteria can have remarkably short cell-doubling times; for example, the doubling time of Escherichia coli K12 can be 20 minutes. For these growth rates, replication of the chromosome can barely keep up with cell division and multiple replication forks in the chromosome are necessary. Most bacteria also contain small, additional nuclear elements called plasmids or extrachromosomal elements. These can be transferred from one cell to another by processes called transformation and conjugation so that additional genes are constantly being exported between bacteria. Through this mechanism, genes conferring traits such as antibiotic- and heavy metal-resistance factors are frequently conveyed amongst bacteria. Remarkably, this happens not only between similar strains of bacteria but also between dissimilar genera. Transfer by conjugation often requires specialized surface structures, called F-pili, through which the extrachromosomal DNA is thought to pass. Special viruses, called bacteriophages or phages, can also transfer new genes to bacteria. Certain bacteriophages are not always lytic and their genomes (after injection into the bacterium) can lie dormant for long periods of time. These are called lysogenic bacteriophage and, frequently, their DNA can integrate into the bacterial chromosome where it replicates and is transferred to daughter cells during binary ssion. Bacterial ribosomes are smaller than the eukaryotic variety (70S versus 80S) and consist of a small 30S subunit attached to a larger 50S subunit. Both subunits consist of a number of separate proteins which are integrated with ribonucleic acid (rRNA) to produce a particle that can be visualized by transmission electron microscopy (Figure 2). Ribosomes are scattered throughout the cytoplasm and are frequently aligned on the inner face of the plasma (cytoplasmic) membrane where they are called polysomes. Both ribosomal varieties are in close contact with the nucleoid (this ensures quick, ecient transcription! translation! protein synthesis) so that rapid metabolic
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Figure 1 (a) Photograph of a piece of the gunflint chert from the northern shore of Lake Superior, Ontario, Canada. The rock measures about 20 cm along the long axis and the wavey striations of the layers of an ancient $ 3000 million-year-old stromatolite can be seen in the middle of the rock. (b) Bright-field light micrograph of a thin section of the gunflint chert showing the mineralized remains of prokaryotic cells. (c) Light micrograph using phase optics of a living modern-day biofilm from a stream in southern Ontario for comparison with (b). These figures were originally supplied by F.G. Ferris, University of Toronto and are reprinted from Beveridge (1988) with permission of the Canadian Journal of Microbiology.

rates are possible. Polysomes are attached to the plasma membrane so that protein translation (to the periplasm) and secretion (to the outside) can occur. The cytoplasm is bounded by a plasma membrane (Figure 2; this is similar to the cytoplasmic membrane in eukaryotic cells but, by convention, is usually called the plasma membrane as coined by early light microscopists).
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This membrane is a lipid/protein bilayer which is semipermeable and which contains a large number of functional enzymes. One common trait of this membrane is that it is energized; there is an electron ow through it and the membrane (usually) pumps protons (H 1 ) from the cytoplasm to the periplasm. This membranes semipermeability enriches the cytoplasm with a relatively high

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Bacterial Cells

Figure 2 Electron micrograph of a thin section of Leptothrix discophera which shows many structural attributes of a bacterial cell. This is a Gram-negative cell and the inner bilayer of the cell envelope is called the plasma membrane which encloses the cytoplasm. Reprinted from Beveridge (1988) with permission of the Canadian Journal of Microbiology.

concentration of organic and inorganic ions so that, by diusion, a water gradient develops between the cytoplasm (high) and the outside (low). Consequently, a large turgor pressure (usually between 3 and 25 atmospheres) pushes against the plasma membrane; this is so formidable that the bilayer would burst unless additional boundary layers (e.g. a cell wall) were added for additional support. These additional layers are discussed in more detail below. The uid of the cytoplasm, in which particulate matter oats (such as the ribosomes and chromosome), is called the cytosol.

Specialized Internal Structures

Usually, there are few cytoplasmic structures in bacteria. When they are found, it is because they possess a distinct functional attribute that is necessary for that particular cell. For example, some bacteria possess small, singledomain granules of magnetite (Fe3O4) aligned to the long

axis of the cell (Figure 3). These membrane-bound particles are called magnetosomes and are the smallest possible form of magnetite that has a magnetic moment. Their linear alignment in a cell converts the bacterium into a small compass needle so that it must align to the geomagnetic eld. For those bacteria residing in the temperate zones (either north or south) of the Earth, the geomagnetic alignment points the cells downwards so that they can migrate towards the microaerophilic (low oxygen tension) conditions they prefer. Other bacteria produce intracellular granules to assist their nutritional needs. For example, glycogen granules are developed by some bacteria as quick-energy reservoirs. Glycogen is a polymeric carbohydrate that can be easily drawn-on by the cell when it is under carbon limitation. Polyhydroxyalkanoate granules (Figure 2; usually consisting of b-hydroxybutyrate, b-hydroxyvalerate or copolymers of the two compounds) can also be found in some bacteria and these are a source of energy which can be drawn-on under longer periods of nutrient limitation. Sulfur granules are found within bacteria (e.g. the purple
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Figure 3 Thin section of a magnetotactic spirillum (a Gram-negative bacterium) which contains a chain of magnetosomes containing small particles of magnetite (Fe3O4). This sample was supplied by D. Bazylinski, University of Iowa.

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Bacterial Cells

sulfur bacteria) that oxidize sulfur compounds. These granules are spread throughout the cytoplasm and are shown to be highly refractile by light microscopy (brighteld or phase) and transmission electron microscopy. As long as these bacteria have a supply of reduced sulfur in their environment, the granules continue to grow as more and more elemental sulfur is laid down. But, as this supply dwindles, the granules become oxidized (usually to sulfate) and are reduced in size. Many bacteria accumulate reserves of phosphate during growth since they require it for highenergy compounds to drive metabolic processes and for structural constituents (e.g. for membrane phospholipids and chromosomal DNA). In this case, the stored phosphate is partitioned into small cytoplasmic polyphosphate granules, which are readily stained by basic dyes used for light microscopy. This metachromatic (or colour) change makes the particles visible and accounts for their other name, metachromatic granules. Bacteria living in aqueous environments sometimes need to alter their ability to oat. These cells produce a most interesting internal otation device called a gas vesicle. The vesicles are constructed of proteinaceous subunits with high b structure that assemble with one another to form a hollow elliptical structure (it resembles a rugby football) about 300600 nm 100 nm. The t of the subunits is so tight that the cytosol cannot pass through; only gases (dissolved in the cytosol) can pass into the lumen of the vesicle, where they collect and concentrate to produce $ 1 atmosphere of pressure. Gas vesicles can regulate the level at which a bacterium oats within a natural water column since the gases within a vesicle eect the cells buoyancy. This can be important for phototrophs (such as cyanobacteria) which depend on discrete wavelengths of light to grow. The light-harvesting apparatus of phototrophs can be shaped into a range of dierent structures but there is always a common characteristic: the photosynthetic pigments are embedded in a lipid bilayer or nonunit membrane which has been derived from the plasma membrane. Cyanobacteria, such as Synechococcus spp., arrange their photosynthetic bilayers as concentric lamellae underneath the plasma membrane (Figure 4a), whereas Chlorobium spp. (green sulfur bacteria) partition their bacteriochlorophylls within cigar-shaped chlorosomes (which are bounded by nonunit membranes) arranged at the cytoplasmic periphery (Figure 4b). Those phototrophs that x carbon dioxide via the Calvin cycle require the enzyme ribulose bisphosphate carboxylase (Rubisco) which is frequently found in carboxysomes (Figure 4a). Bacteria that require other dedicated enzyme systems for their growth in particular ecological niches also frequently partition these enzymes into intracellular membranes. For this reason, nitriers (e.g. Nitrosococcus) and methanotrophs (e.g. Methylococcus) typically use such membranous structures.

Shape and Form

The characteristics of shape and form are of extreme importance to bacteria. Bacteria cannot reach out and grab hold of food nor can they engulf it. Instead, they must rely on diusion in the outside environment to bring food to them and to take waste materials away. Therefore, anything they can do to encourage diusive processes will be helpful. Simple design modications that aect shape can be quite advantageous. For example, a coccus (such as Staphylococcus) has a low surface area-to-volume ratio; there is not much surface area for adsorption of nutrients compared to the relatively large volume of cytoplasm to be nourished. Yet, if a cell of similar volume is converted to a rod (e.g. Bacillus), the surface area (and adsorption) is drastically increased. Supposedly, this is one of the reasons why B. subtilis can outgrow S. aureus under similar growth conditions. In the microbial world, a number of dierent bacterial shapes are encountered (e.g. spheres, rods, commas, spirals, prosthecate (Figure 5), etc.) and the trend towards a greater surface area-to-volume ratio for better exchange of nutrients and wastes must be a potent selective driving force.

Biofilms
In natural settings, it is not uncommon to nd most bacteria attached to interfaces where they form so-called biolms. In aqueous habitats, the airwater interface and solid surfaces are preferred because they tend to accumulate nutrients as a result of adsorptive and interfacial eects. Bacteria take advantage of these collected nutrients, adhere to the surface, grow and divide. Soon, they outgrow one another, microbial consortia become interdependent (some cells require cofactors or metabolic substrates produced by others) and stratication occurs (nutrient, pH and redox gradients develop). Here, cell shape is still important. Caulobacter, which is a prosthecate bacterium, attaches its stalk to the substratum by means of a proteinaceous glue on the holdfast of its stalk (Figure 5). Once fastened, the stalk gradually lengthens as the biolm (composed of other bacteria) thickens. This keeps the Caulobacters cell body in the biolms outer reaches where oxygen and nutrients are plentiful. Here too, chains of lamentous cyanobacteria grow by orienting their laments (chains of cells) to the surface of the biolm so that they contact sunlight. As these natural aquatic biolms ourish they become thicker, the innermost regions becoming anoxic, encouraging the growth of anaerobes.

Enveloping Structures
In the Bacteria, all cells except the Mollicutes (the so-called wall-less bacteria) have additional structural layers above
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Figure 4 (a) Thin section of the cyanobacterium Synechococcus GL-24 showing the concentric arrangement of the photosynthetic membranes and the carboxysomes. (b) Thin section of a Chlorobium sp. which is a green sulfur bacterium showing the photosynthetic chlorosomes. Both (a) and (b) were provided by S. Douglas, University of Guelph and (a) is with permission of the Journal of Bacteriology.

the plasma membrane. The number and type of extra layering depends on the variety of bacterium, but almost all possess a cell wall immediately above the membrane. Gram-positive bacteria possess a thick wall (usually $ 2030 nm thick) composed of peptidoglycan and secondary polymers, usually consisting of teichoic acid, teichuronic acid, or both polymers. Peptidoglycan is the primary structural component because its individual glycan strands are covalently linked to immediately adjacent strands, thereby forming a bonded network completely surrounding the cell. This network can be 20 or more molecular layers thick. It is a strong network and is necessary to resist the cytoplasmic turgor pressure discussed in a previous section. The secondary polymers are attached to and intercalated with the peptidoglycan network so that an amorphous matrix (i.e. the Grampositive cell wall) results. Gram-negative walls are more complex (Figure 2). They too have peptidoglycan, but in much smaller amounts.
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This network is only 13 molecular layers thick and resides above the plasma membrane in the periplasmic space. Immediately above is the outer membrane, consisting of a lipid/protein bilayer of dierent composition to that of the plasma membrane. Several of the major proteins (outer membrane proteins or OMPs) assemble together into multimers which span the bilayer, forming aqueous channels connecting the outside to the underlying periplasmic space. The outer membrane is one of the few biological membranes to have an asymmetric distribution of lipid. The inner face contains phospholipid, whereas the outer face contains lipopolysaccharide (LPS). The region between the outer and plasma membranes, the periplasmic space, is lled with a concentrated brine of organic molecules. Many of these are enzymes responsible for a full range of activities including the breaking down of large nutrients to smaller ones essential for metabolism, conveying essential vitamins and minerals to the cell, and detoxifying harmful agents.

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Figure 5 Electron micrograph of a negatively stained Caulobacter sp. showing its unusual shape complete with stalk and holdfast. Reprinted from Beveridge (1988) with permission of the Canadian Journal of Microbiology.

Additional layers above the cell wall can often be found. Sometimes a gel-like matrix can be produced; if it is attached to the cell wall it is called a capsule (Figure 2), if not, it is a slime. Both extracellular polymeric substances are frequently found separating individual cells in biolms. Another capsule-like structure in which chains of cells can reside is a sheath. This is a cylindrical structure that sometimes is the outermost boundary layer of Leptothrix, Sphaerotilus, Beggiatoa and cyanobacteria (Figure 2). S layers are more ordered structures that can be encountered attached to cell walls. These consist of proteins (or glycoproteins) which interact with each other once they reach the wall surface so that they self-assemble in regularly ordered, planar arrays (Figure 4). These paracrystalline arrays, or S layers, can be arranged in oblique (p2), square (p4) or hexagonal (p3, p6) lattices.

Gram-staining Properties
The structural format and chemical composition of bacterial cell walls dictate the staining response of cells to the Gram stain. This stain for bright-eld light microscopy was formulated by Christian Gram in 1884 and is still a prime method for distinguishing dierent types of bacteria during their taxonomical identication. Bacteria are heatxed to a glass slide and stained with crystal violet (purple) for 60 s. Grams iodine (containing potassium iodide) is next added as a chemical mordant for 180 s. The slide is rinsed with a steady ow of ethanol for 20 s and, lastly, the cells on the slide are stained with safranin (red) as a counterstain for 60 s. Crystal violet enters all bacteria and stains them purple. Grams iodine clusters the stain into large precipitates that cannot be removed from the cell unless the cell wall is broken down. When the ethanol rinse is applied to the slide, the cell wall of Gram-positive bacteria is not aected,
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Bacterial Cells

the crystal violet cannot be removed from its intracellular location and the cells remain purple. Gram-negative bacteria, however, are decolorized by the ethanol rinse. Since the outer and plasma membranes dissolve in alcohol, the crystal violetiodine complex is washed away and the safranin counterstain dyes the bacteria red. Safranin does not aect the purple colour of Gram-positive cells when it is applied.

Motility Structures
The most common type of motility in bacteria is swimming. Here, one or more agella rotate to push (or pull) the cell through an aqueous milieu. The bacterial agellum consists of a long spiral lament (Figure 6) made up of a helical arrangement of proteins referred to as agellins. The lament is $ 20 nm thick, can be one or more cell lengths long and is hollow (so that newly synthesized monomeric agellin can migrate through the hollow cavity from the cell body to the distal tip of the agellum where it self-assembles). Most laments consist of only one variety of agellin (e.g. Escherichia coli), but some have two or more agellins (e.g. Campylobacter and Vibrio). The lament is attached to a hook which is connected to a basal body (Figure 6). The basal body is a complex organelle that attaches the agellum to the cell body and is constructed of a number of structural parts. In Gramnegative bacteria, it consists of a rod with attached rings; the L ring is inserted into the outer membrane, the P ring is aligned with the peptidoglycan layer, and the S-M ring is embedded into the plasma membrane. A proton gradient across the plasma membrane is the driving force which rotates the S-M ring and, thus, rotates the entire agellum, acting as a propeller and driving the bacterium forward. As explained in a previous section, Gram-positive bacteria do not have an outer membrane as a structure in

their cell walls, but only a relatively thick matrix of peptidoglycan and secondary polymers. The agella of these bacteria do not, then, have L and P rings in the basal body, but only the S-M ring. Rotation of Gram-positive agella is by the same mechanism as explained for Gramnegative cells. There are some variations from this general theme. Some bacteria possess only one agellum and often this is at a single polar location on the cell (e.g. Pseudomonas aeruginosa). This arrangement is called monotrichous (i.e. single hair). Others can have tufts of agella at one or both poles (e.g. Aquaspirillum serpens; such an arrangement is called lophotrichous (i.e. tuft hair)). Those bacteria with agella placed continuously around the cell body (e.g. E. coli) have a peritrichous arrangement (i.e. [all] around hairs). Vibrio and Bdellovibrio have sheathed agella in which the lipidprotein bilayer of the outer membrane extends over the length of the agellum. Spirochaetes, such as Treponema pallidum, have adopted an entirely dierent strategy by burying their agella in the periplasm, aligning them along the cell axis so that these endoagella are never exposed to the outside. Two other types of motility have been described for bacteria: twitching and gliding. Twitching is the result of contractile pili (also called mbriae) and this motility system seems to be nondirectional and has not been extensively studied. Gliding has been better studied and requires an interface (usually a solid surface) for the bacteria to move on. By inference, this motility system must (somehow) push or pull on the substratum surface and a number of propulsion devices have been proposed (i.e. directed extrusion of exopolymers, surface active agents, small rotating discs, moving brils, etc.). So far, the exact nature of gliding motility is unclear.

Figure 6 Negative stain of the proximal end of a flagellum from Campylobacter fetus subsp. fetus which shows the filament, hook and basal body (L, P and S-M rings).

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Figure 7 Thin section of a Bacillus megaterium endospore.

Specialized Structures for Survival

The best-studied survival structure for bacteria is a resting cell called an endospore. This is a highly resilient cell that is formed within a mother cell. It is encased in a number of robust coatings and has almost no detectable metabolism (Figure 7). As the endospore forms, much of the cytoplasmic water is removed, a specialized substance (dipicolinic acid) is synthesized to complex Ca2 1 , and special coatings are laid down. For the latter, a thick peptidoglycan-containing cortex is formed rst above the plasma membrane of the spore. Next, the spore coat (consisting of a regular arrangement of high cysteine-containing proteins) appears, followed by a more loosely arranged exosporium. At this point, the cytoplasm of the spore has lost so much

water it has become very dense and its metabolic processes barely detectable; this region is now called the core. Using light microscopy, endospores are highly refractile. Endospores are highly resistant to desiccation, poor nutrition, extremes in temperature, harsh chemicals, extreme pH and radiation, and can survive under such stressful conditions for long periods of time. Once they encounter better environments, they germinate; their robust encompassing garments break open and a vegetative cell emerges; this is called outgrowth. Endospores are most frequently encountered in Bacillus and Clostridium spp. Azotobacter produces another type of resting cell called a cyst. These are also produced during harsh conditions but, in this case (unlike an endospore), a cyst is not produced
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within a mother cell. The mother cell itself begins to dehydrate and brous material is laid down outside of the outer membrane of this Gram-negative bacterium. Eventually, this brous material arranges itself as concentric layers around the cell body and can be $ 0.5 mm thick. As this is happening, large polyhydroxyalkanoate granules (as carbon reserves) begin to take up much of the cytoplasmic volume. More recently, there has been a general recognition that many Gram-negative bacteria under nutrient limitation in natural environments have another strategy for survival. They gradually cannibalize themselves until only the bare essential structures are left. By doing this they become drastically reduced in size, contain few ribosomes, possess a condensed chromosome and are bounded by a typical Gram-negative envelope. These small cells can remain in this state of stasis until conditions become more favourable. They are referred to as ultramicrobacteria or nanobacteria.

Concluding Remarks
This article serves as a general introduction to the structure of bacteria. Because it strives to encompass many of the structures found in this large prokaryotic domain it cannot present all the details. It should be remembered that not all bacteria possess all of the structures mentioned in this article. Many are species- or genus-specic, whereas others are induced by environmental factors.

Further Reading
Beveridge TJ (1981) Ultrastructure, chemistry and function of the bacterial cell wall. International Review of Cytology 72: 229317. Beveridge TJ (1988) The bacterial surface: general considerations towards design and function. Canadian Journal of Microbiology 34: 363372. Beveridge TJ (1989) The structure of bacteria. In: Poindexter JS and Leadbetter ER (eds) Bacteria in Nature: A Treatise on the Interaction of Bacteria and their Habitats, pp. 165. New York: Plenum Publishing. Beveridge TJ (1990) Mechanism of Gram variability in select bacteria. Journal of Bacteriology 172: 16091620.

Beveridge TJ (1994) Bacterial S-layers. Current Opinion in Structural Biology 4: 204212. Beveridge TJ and Davies JA (1983) Cellular response of Bacillus subtilis and Escherichia coli to the Gram stain. Journal of Bacteriology 156: 846858. Beveridge TJ and Graham LL (1991) Surface layers of bacteria. Microbiological Reviews 55: 684705. Beveridge TJ and Schultze-Lam S (1997) The response of selected members of the Archaea to the Gram stain. Microbiology 142: 2887 2895. Beveridge TJ, Makin SA, Kadurugamuwa JL and Li Z (1997) Interactions between biolms and the environment. FEMS Microbiology Reviews 20: 291303. Costerton JW, Cheng K-J, Geesey GG et al. (1987) Bacterial biolms in nature and disease. Annual Reviews of Microbiology 41: 435464. Davies JA, Anderson GK, Beveridge TJ and Clark HC (1983) Chemical mechanisms of the Gram stain and synthesis of a new electron-opaque marker for electron microscopy which replaces the iodine mordant of the stain. Journal of Bacteriology 156: 837845. Koch AL (1995) Bacterial Growth and Form. New York: Chapman and Hall. Ko nig H and Messner P (special eds) (1997) 4th International S-layer Workshop (Rothenburg o.d. Tauber, Germany). FEMS Microbiology Reviews 20: 5175. Macnab RM and DeRosier DJ (1988) Bacterial agellar structure and function. Canadian Journal of Microbiology 34: 442451. Messner P and Sleytr UB (1992) Crystalline bacterial cell surface layers. Advances in Microbial Physiology 33: 213275. Poindexter JS and Leadbetter ER (eds) (1989) Bacteria in Nature: A Treatise on the Interaction of Bacteria and their Habitats, vol. 3. New York: Plenum Publishing. Salton MRJ (1963) The relationship between the nature of the cell wall and the Gram stain. Journal of General Microbiology 30: 223235. Walter MR (1983) Archean stromatolites: evidence of the earths earliest benthos. In: Schopf JW (ed.) Earths Earliest Biosphere: Its Origin and Evolution, pp. 187213. Princeton: Princeton University Press. Whiteld CW (1993) Biosynthesis and expression of cell-surface polysaccharides in Gram-negative bacteria. Advances in Microbial Physiology 35: 135246. Wilson DR and Beveridge TJ (1993) Bacterial agellar laments and their component agellins. Canadian Journal of Microbiology 39: 415 427. Woese CR, Kandler O and Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proceedings of the National Academy of Sciences of the USA 87: 45764579.

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