Audio recording of this lecture

Previous or Next lecture

Spirochaetes and Bacteroids

The phyla Spirochaetes and Bacteroids contain many common but generally unfamiliar organisms. Although the Spirochaetes bring to mind some important pathogens, both groups are common in the environment and as components of the normal flora of animals. Although not specifically related, nor alike morphologically, these two groups share a common metabolic theme; most are saccharolytic, and are often involved in the decomposition of long-chain polysaccharides such as cellulose and chitin. In addition, each group is motile by a mechanism different that the common flagellar propellor most commonly found in Bacteria.

Phylum Spirochaetes

Taxonomy

• Phylum Spirochaetes
  • Class Spirochaetes
    • Order Spirochaetales
      • Family Spirochaetaceae
        • Genus Spirochaeta
        • Genus Borrelia
        • Genus Brevinema
        • Genus Clevelandina
        • Genus Cristispira
        • Genus Diplocalyx
        • Genus Hollandina
        • Genus Pillotina
        • Genus Treponema
      • Family Serpulinaceae
        • Genus Serpulina
        • Genus Brachyspira
        • Genus Serpula
      • Family Leptospiraceae
        • Genus Leptospira
        • Genus Leptonema
        • Genus Turneriella

About this phylum

Diversity
Most of familiar organisms in this group (the pathogens and their relatives) are closely-related members of the family Spirochaetaceae. Many species that were originally thought to be members of this group, even species of the genera Spirochaeta and Treponema have more recently been shown by phylogenetic analysis to constitute a separate group, the Family Serpulinaceae. This Family is known primarily for animal and human intestinal parasites. The environmental species are more diverse, and because they are typically difficult to grow, even most of the conspicuous species have not been grown or studied in culture, and so their phylogenetic affiliations are generally unknown.

Metabolism
The spirochaetes are uniformly heterotrophs and generally microaerophilic or anaerobic and saccharolytic, although some ferment amino acids (e.g. Treponema denticola, a member of the normal flora of human teeth and gingiva). H2 and CO2 are the main products of this fermentation, although some can convert these two waste products to acetate. In contrast, the leptospiras are generally aerobic degraders of fatty acids.

Morphology

The spirochaetes share a common body plan. The long, thin body of the cell is generally helical or a two-dimensional wave. Polar flagella (typically one at each end, but more are present in the larger species) are anchored subterminally in the cytoplasmic membrane but do not emerge from the outer membrane; they are contained in the periplasm. These flagella wind their way along the curved or helical shape of the cell body, usually overlapping in the medial part of the cell. Flagellar rotation causes the body of the cell to rotate within the outer membrane. In flat wavy species, this will cause the cell to move across a surface or through a liquid environment similar to the way a snake moves along the ground or in the water. This also works for helical species because the viscosity of their surroundings retard rotation of the outer membrane surface; the shape of the cell therefore rotates like a corkscrew, providing propulsive force.

Habitat
Spirochaetes are common sediment inhabitants, especially in those rich in decomposing plant material, in which they are involved in the decomposition of cellulose and other polysaccharides. The best-studied spirochaetes, however, are symbionts or parasites of the gastrointestinal tract of animals, including humans. A few parasites (e.g. Treponema pallidum) invade the tissues of the host, but most inhabit the surface of the mucosa. The richest, most readily available source of samples containing large numbers of spirochaetes are the hindguts (homologous to the colon of vertebrates) of wood-eating insects, especially termites.

Are Spirochaetes the progenitors of eukaryotic flagella?

Termites and other wood-eating insects subsist primarily on a diet of cellulose. The degradation of cellulose and the generation of the nutrients required by the insect is an involved process carried out by a complex population of symbiotic Bacteria (including spirochaetes), Archaea (methanogens), and eukaryotes (protists). Some of the protists involved harbor symbiotic spirochaetes, which are attached to the surface of the protists at one end of their wavy or helical cells. Movement of the this “collective” is driven by movement by the spirochaetes, but apparently directed by the protist. The spirochaetes greatly resemble flagella or long cilia, to the extent that in many cases it is difficult to distinguish normal flagella born by the protist from symbiotic spirocheates attached to the same creature. This similarity in form and function lead to the suggestion that eukaryotic flagella, and the associated structures including cilia, basal bodies, and the spindle apparatus, all hallmarks of the eukaryotic cell structure, may have originated by symbiosis of a progenitor eukaryote with a spirochaete. We know this is the case for the origin of mitochondria (by symbiosis with an α-proteobacterium) and plastids (by symbioses with cyanobacteria). However, unlike mitochondria or plastids, neither flagella nor their associated cellular structures contain DNA, nor is their evidence for the transfer of significant numbers of spirochaete genes into the nuclear genome. Neither do the cytoskeletal structures of spirochetes nor their periplasmic flagella resemble in structure, mechanism, or molecular sequence the tubulin/microtubule structures of eukaryotic flagella or their associated structures.

Spirochaetes

The familiar genera in this Family are Spirochaeta (free-living species), Treponema (animal symbionts and pathogens) and Borrelia (human pathogens with arthropod vectors). These species are anaerobic, microaerophilic or facultatively aerobic. The cultivated Spirochaeta and Borrelia are saccharolytic. Cultivated Treponema are also generally saccharolytic, but a few can grow on fatty acids or amino acids and most have not been grown in pure culture and so their growth substrates are not known. Linear (rather than circular) genomes and plasmids are common in this group.

Example: Treponema denticola

Although this genus is best known for the important pathogen Treponema pallidum, treponemes are common in the mouth and GI tract of healthy humans and other animals. The pathogenicity of T. denticola is not clear; it is found in dental plaque and gingiva of healthy human teeth (and those of other primates), but are more abundant in people and teeth affected by gingivitis. Although usually described as helical in shape, this specie is probably a 2-dimensional wave like its close relative, T. pallidum. Unlike most spirochaetes and treponemes, T. denticola is strongly proteolytic, and so presumably is capable of fermentation of amino acids in its natural environment.

Example: Borrelia recurrentis

Although the best known Borellia is B. burgdorferi, the causative agent of Lyme disease, a wide variety of Borrelia species cause similar zoonotic infections. B. recurrentis is the cause of louse-borne relapsing fever. This relapsing fever is caused by the organisms use of antigenic variation to evade elimination by the hosts immune response. Like other species of this genus, the ends of the cells are tapered to fine points. Cells are relatively open helices, and contain 8-10 periplasmic flagella. Although it has not been tested in the case of this specie, other species of Borellia have linear genomes.

Leptospiras

In contrast to the other spirochaetes, the leptospiras are obligately aerobic and use fatty acids as their growth substrate. Leptospiras are common in the aquatic environments and in association with mammals, including humans. Human pathogenesis is zoonotic; humans are apparently not effective hosts or carriers. Animals carriers harbor the parasites in their kidneys and the transmit the infection via urine. Human infections are primarily those with direct contact with wild or domestic mammals. Leptospirosis is easily confused with other fevers, especially yellow fever. Only two periplasmic flagella are present, and the cells a very thin and tightly coiled, usually with bent or curved ends.

Example: Leptospira biflexa

L. biflexa is a non-pathogenic aquatic specie that is very closely related to several pathogenic and opportunistically pathogenic species, and so serves as a model system for spirochaete virulence. It is also a model system for examining motility in spirochaetes. When moving, the trailing end of the cell is bent in a hook shape, and the leading end forms an open left-handed spiral (over and above the usual right-handed helical cell shape). Both of these rotate as the cell progresses forward. Although rotation of the helical cell body is sufficient to propel the organism through low viscosity environments, the rotation of the hook and spiral ends allow the organism to bore its way through viscous environments efficiently.

Phylum Bacteroids (Sphingobacteria, or Bacteroides/Flavobacterium/Cytophaga group)

• Phylum Bacteroids
  • Class Bacteroidetes
    • Order Bacteroidales
      • Family Bacteroideceae (e.g. Bacteroides, Pontibacter)
      • Family Rikenellaceae (e.g. Rikenella, Alistipes)
      • Family Porphyromonadaceae (e.g. Porphyromonas)
      • Family Prevotellaceae (e.g. Prevotella, Xylanibacter)
  • Class Flavobacteria
  • Order Flavobacteriales
    • Family Flavobacteriaceae (e.g. Flavobacterium, Polaribacter)
    • Family Blattabacteriaceae (Blattabacterium)
    • Family Cryomorphaceae (e.g. Algoriphagus, Cryomorpha)
  • Class Sphingobacteria
    • Order Sphingobacteriales
      • Family Sphingobacteriaceae (Sphingobacterium, Pedobacter)
      • Family Saprospira (e.g. Saprospira, Haliscomenobacter)
      • Family Flexibacteraceae (e.g. Flexibacter, Cytophaga)
      • Family Flammeovirgaceae (e.g. Flexithrix, Persicobacter)
      • Family Crenotrichaceae (e.g Chitinophaga, Rhodothermus)
        

About this phylum

Diversity
This is a very large and diverse phylum, encompassing at least 140 genera. The phylum is composed of 3 major groups, the Bacteriods (Bacteroidetes), Flavobacteria (Flavobacteriales) and Sphingobacteria (Sphingobacteriales, sometimes known as the “Cytophaga and relatives”). Although very common in the environment, there are no spectacular human pathogens or industrial organisms in this phylum, and so they are generally unfamiliar and not well studied. The Spingobacteria are specifically related to the Chlorobi, and are sometimes grouped together into a single phylum.

Metabolism
These organisms are generally saccharolytic, either obtaining sugars directly from the environment or releasing them from long-chain polysaccharides such as cellulose and chitin. The Bacteroids are generally anaerobes, the Flavobacteria and Sphingobacteria are aerobes. Most are naturally resistant to aminoglycoside antibiotics. Members of this group synthesis and incorporate sphingolipids into their membranes. Sphingolipids are otherwise known from the cytoplasmic and vesicle membranes of eukaryotes, but especially those of the nervous system of animals.

Morphology
The Sphingobacteria are rod-shaped cells, typically long and thin and often with slightly tapered ends. The most conspicuous exceptions to this are Bacteroides, which are typical rod-shaped cells, and Sporocytophaga, which are typical thin tapered rods during log-phase growth but form spherical resting spores in stationary phase. Cells are motile by gliding, or non-motile.

Habitat
Sphingobacteria are common in a wide range of environments, especially in soils, sediments, and the gut contents of animals; all environments in which long-chain polysaccharides and their decomposition products are degraded. These organisms are found in both moderate temperatures (mesophiles) and cold environments (cryophiles); thermophiles are not known.

Bacteroids

Bacteroids are obligately anaerobic, non-spore-forming rods. The familiar species in this Family are Bacteroides and Porphyromonas. Bacteroides and similar relatives are non-pigmented and saccharolytic or peptidolytic, preferring complex polysaccharides and producing primarily acetate and succinate as their fermentation products. Unlike most polysaccharide degraders,which secrete hydrolytic enzymes into the environment or onto the outer surface of their cells, Bacteroides transport insoluble particles of polysaccharide into the periplasm for degradation; the sugars released by hydrolysis are transported directly into the cell. Porphyromonas are similar morphologically, but are heavily pigmented with protoheme and protoporphyrin, producing very dark brown or black colonies. Their preferred growth substrate is peptides, which are converted into a wide range of organic acids. Both genera are abundant symbionts of anaerobic mucous membranes of humans and other animals. Although they are considered normal flora, they can also be opportunistically pathogenic. Porphyromonas in high numbers is associated with gum disease and gingivitis.

Example: Bacteroides thetaiotaomicron

B. thetaiotaomicron and related species (e.g. B. fragilis) is a major component of the human colonic flora, comprizing about 1/3rd of Bacteria in feces. (Most of the rest are a variety of Clostridium species.) Gastrointestinal infections caused by Bacteroides are usually caused by a close relative, B. fragilis. B. thetaiotaomicron can degrade and grow on starch, but not other polysaccharides.

Flavobacteria

The Flavobacteria are obligately aerobic, yellow-pigmented rods, usually long rods with slightly tapered ends. They are common in marine and freshwater environments. Most are non-motile, but some can move rapidly by gliding. Some species can hydrolyze chitin, gelatin, or starch if allowed to attach directly to the surface of these polymers. Many are also proteolytic. They are rarely involved in human disease (usually meningitis in infants), but their innate high-level resistance to many antibiotics often results in a dangerous delay in effective treatment. However, they are very important pathogens of fish, especially in aquacultured trout and salmon.

Example: Flavobacterium johnsoniae

F. johnsoniae is a common aquatic (freshwater and marine) chitin-degrading organism. It is a rapid glider; up to 10μm per second, which is often mistaken for flagellar motility. However, this gliding motility requires contact with the substrate; they are incapable of swimming. It is a model system for the study of the unusual mechanism of gliding motility in Bacteroids. Interestingly, non-motile mutants of F. johnsoniae are all also incapable of chitin degradation, implying a link between these processes; the nature of this link is not understood.

Sphingobacteria

Cytophaga and relatives are typically long thin flexible rods, but vary from short rods to filaments or open spirals. Motile by gliding these organisms are capable of degrading a wide range of biopolymers: chitin, agar, starch, cellulose, pectin, nucleic acids, and proteins. These organisms are abundant in nutrient-rich aquatic environments, sediments and soils. Some are pleomorphic, forming rod-shaped or filamentous cells during log phase growth, and spherical or short rod-shaped spores in stationary phase. Cultures of these pleomorphs are often thought to be contaminated because of the different distinct cell morphologies. Colonies are usually feathery as a result of cells streaming on the agar surface. Cells placed on glass slides (e.g. in a wet mount) are often arranged in side-by-side monolayers.

Example: Cytophaga hutchinsonii

C. hutchinsonii is a long flexible rod-shaped cellulose degrader from soil. Cellulose degradation requires the organisms to be in direct contact with the substrate; extracellular cellulases are not produced. Cells adhere to cellulose, and orient themselves and glide along the axis of the cellulose fibers. Only cellulose and its decomposition products cellobiose and glucose can sustain growth; other simple monoacchrides (except gluconate) cannot be used.

Bacterial motility

Most Bacteria have the ability to move from one place to another in at least some part of their life cycle. The most common and best-understood form of motility is that driven by flagella, but many mechanisms of motility are used by Bacteria, and in some cases a specie may be capable of more than one type of motility.

Although only well-studied in a few flagellated organisms, the che gene signaling pathway for chemotaxis are widespread in Bacteria, and the same process probably regulates chemotaxis in other organisms regardless of their method of motility.

Flagella

A wide range of Bacteria are motile via flagella. Flagella are proton-gradient-driven helical propellers, allowing the organism to “swim” through an aqueous environment. Cells can have one to many flagella, located at one or both ends or distributed all over. A rare arrangement is to have flagella only on one side of a rod-shaped cell - these cells swim sideways, counter-rotating like a propeller.

Some flagellated organisms are curved (vibrios) or spiral-shaped (spirilla). This increases the efficiency of flagellated motility, despite the increase in surface area. Viscous resistance on the rotating flagella cause a counter-rotation of the cell body; if the cell is properly curved, this lost energy is recaptured by turning the cell into a screw.

Cells 'run' (move continuously in a more-or-less straight line) when the flagella turn one direction, and 'twiddle' (tumble) when they turn the other direction. The length of a run is dependent of whether the cell is moving in the desired direction - long runs if so, short runs if not. Twiddling reorients the cell randomly between runs. The result in a directed random walk - a fairly efficient way to get where you want to go.

Spirilla are little different - they typically have polar flagella, and "twiddle and run" like other flagellated organisms, but usually switching from running the flagella and one end of the cell to the other end of the cell after each twiddle. They can also switch back and forth between running the flagella at either end of the cell without twiddling, resulting in the cell running directly back and forth. They also use this ability to quickly reverse directions when they run into something, or come into abrupt contact with a repellant.

Gliding

Gliding motility is accomplished by at least two fundamentally different mechanisms.

Cyanobacteria, Chloroflexi, Thiotrichs and probably Myxobacteria, and many eukaryotic algae, glide using a mechanism that involves the secretion of polysaccharides from pores on cell surface. Hydration of the polysaccharide as it emerges into the aqueous environment causes it to expand dramatically and provides a reactive force much like a rocket engine. Unicellular gliders usually have the pores at each end of the cells (which are typically rods). Filamentous gliders have these pores along the leading and trailing edges of individual cells, oriented fore and aft.

How cells control which pores to activate, so that the cells move in one direction or the other, is not known. Nor is the coordination of motility between cells of a filament understood. Gliding leaves a polysaccharide 'slime' trail stuck to a substrate or hanging in solution, and is an efficient a way to move over the surface of a solid material as well as through liquid media.

The Bacteroids glide using a very different and poorly understood mechanism. Adhesins on the surface of the cells seem to move uniformly from one end of the cell to the other. Presumably the adhesins are internalized upon reaching the trailing end of the cell, and reemerge at the leading edge. Think of the tracks on a bulldozer, a conveyor belt, or an escalator. These organisms can only glide if in contact with a surface. It has been proposed that gliding in Myxobacteria may be similar, except that the surface adhesins follow a helical path along the surface of the cell, guided by the cytoskeleton.

Gliding in Mycoplasma is poorly understood, and may be based on two different unique mechanisms. Rapid gliding in some Mycoplasma species may be the result of protein “legs” on the leading appendage of these organisms. Slow gliding in other Mycoplasma species may involve surface adhesins and “inchworm” extension and contraction of the leading appendage.

Twitching

A few organisms, such as Myxobacteria (which also glide) and some species of Pseudomonas (which can also produce flagella), Neisseria, Nostoc and Clostridium can move across surfaces using retractable pili. Think of this as grappling-hook motility; the cell extends a pilus (type IV, where it has been determined) in the direction it wants to move, the end of the pilus attaches to the substrate, then retraction of the pilus pulls the cell forward, generally a few cells lengths at a time. Each pull looks like a 'twitch', thus the name. Some types of cells can produce many pili simultaneously, so that the cell can more usually move more-or-less smoothly forward, looking a lot like gliding, for which this is often mistaken. In order to change direction, the cell has to disassemble the pilus apparatus from one end and reassemble it at the other - and, again, the mechanism for this is not at all understood.

Gas vacuoles

Many aquatic phototrophs move themselves up and down in the water column by fine-tuning their buoyancy using gas vacuoles. These can be bound by a lipid membrane similar to the cytoplasmic membrane, or by a protein layer. Gas vacuoles usually contain CO2 generated by metabolism. Gas vacuoles are very rigid structures, and do not compress or expand significantly over a wide range of pressures; this helps simplify maintaining constant buoyancy. Otherwise, the gas expansion during ascent or compression during descent would require the organisms to constantly adjust their buoyancy, a problem well known to SCUBA divers.

Spirochaete motility

Spirochaetes move by rotation of periplasmic flagella. This method of motility is therefore structurally related to flagellar motility, but is mechanistically very different. Rotation of the periplasmic flagella cause the rigid helical cell body to rotate within the outer membrane. Viscous resistance with the surrounding media prevents the outer membrane from spinning freely. As a result, the shape of the cell relative to the surrounding media forms a rotation corkscrew, as so drives the cell forward.

Not all spirochaetes are helical; many are flattened waves. The same mechanism caused the shape of the cell to wave and progress forward much in the same way that a snake moves forward on flat ground. In some cases, spirochaetes are bent or curved at the ends (see Leptospira, above) to improve motility through semisolid environments, such as the interstitial spaces between animal host cells.
Spirochaetes run when the two terminal flagella rotate in opposite directions (i.e. together, since they are from opposite ends of the cell). The cell can switch the direction of motion by switching the rotation of both flagella simultaneously. If the switch is not simultaneous, the cell flexes while the flagella rotate out-of-sync, analogous to the twiddles of other bacteria.

Spiroplasma motility

Spiroplasma is a relative of Mycoplasma. Spiroplasma cells are helical, and move by a novel mechanism based on changes in shape of its internal cytoskeleton. This cytoskeleton is a flat ribbon composed of 14 fibrils (7 pairs) that is fixed to the inside surface of the cells along the midline of the cell spiral. Independent contraction of the fibrils in this cytoskeletal ribbon can be used to contract or expand the helical shape of the cell, or even reverse the handedness of the helix, at any point along the length of the cell. Motility is driven by moving a stretched or contracted region of the cell, or a kink produced by a short region of reversed handedness, in a wave from one end of the cell to the other; viscous drag on this irregularity in the helix results in rotation of the cell, which drives it forward.



Questions for thought

• At the size scale of Bacteria, momentum is trivial but viscosity is very high, i.e. the Reynolds number is low. From the perspective of a bacterium, they and everything around them are essentially massless, but water has the consistency of cold molasses. How does this affect how you might think about the different forms of motility described above?
  
  
• What do you think of the hypothesis that eukaryotic flagella might be derived from spirochaetes? How would you test this hypothesis? What observations would confirm or refute this hypothesis in your mind?
  
  
• What do you see the relative advantages and disadvantages of each type of motility to be?
  
  
• Can you think of any other mechanism Bacteria might be able to exploit for motility?

Previous or Next lecture