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Phylum Nematoda ( with some pics removed ). "If all the matter in the universe except the nematodes were swept away, our world would still be dimly recognizable... we would find its mountains, hills, valleys, rivers, lakes and oceans represented by a film of nematodes."

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phylum nematoda with some pics removed

Phylum Nematoda(with some pics removed)

"If all the matter in the universe except the nematodes were swept away, our world would still be dimly recognizable... we would find its mountains, hills, valleys, rivers, lakes and oceans represented by a film of nematodes."

Nathan Augustus Cobb, 1914

PJA Shaw

general introduction
General introduction
  • The commonest of the “pseudocoelomates” (note that this taxon is now polyphyletic so invalid) are the roundworms nematoda - from nema - a thread, eidos - form.

Nematodes are ubiquitous in sediments, soils, and bodies. Most are c. 1mm long, with a tiny number of giants. The human gut hosts Ascaris lumbricoides, up to 20cm long in females while the guinea worm Dracunculus medicensislives in our flesh and may exceed 1m. Dogs have the misfortune to host the dog kidney worm Dioctophema renale, 1.2m long and 1cm diameter, while the record comes from a parasitic nema confined the the placenta of sperm whales Placentanema gigantissima, recorded up to 7m long!

basics
Basics..

Formally they are bilaterally symmetrical, vermiform. Their body has well defined tissues and organs. They have a thick complex cuticle underlain by longitudonal mucles (but no circular muscles), a pseudocoel, and a single cell-layered gut running from the anterior mouth to a subterminal anus. The pharynx is strongly muscular, with a triangular cross section, and sucks in liquid / micro-particulate food. There is no circulatory system, and the excretory system is very basic (neither flame cells nor nephridia, but unique structures called renette cells.).

Almost all have the same body shape - round, pointy at both ends, with very few exceptions. Some species have hair-like spines or setea coming off the body wall. A very few plant parasitic species look like balloons, being immobile and full of eggs.

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Despite high levels of morphological homogeneity, nematodes are one of the most successful phyla on the planet. They have colonised every damp habitat yet studied, and their species richness is still poorly understood.

Approximately 15,000 species are described, but estimates of species yet to be discoevered run into excess of a million. These high figures come largely from recent work on the nematodes of sea-floor sediments at great depths, which have revealed remarkable levels of species richness.

There is a school of thought that each species of animal has at least one species-specific nematode parasite, therefore nematodes must outnumber all other species - this argument depends crucally on the host-specificity of coleoptera-parasitic nemas of tropical forests (why?) about which virtually nothing is known.

cuticle
Cuticle

Arguably the defining feature of the nematode body is its thick cuticle. All nematodes have a thick collagen body wall retaining a high internal hydrostatic pressure, up to half an atmosphere - they are almost impossible to squash under normal circumstances. The design of the body wall is unique to the phylum. It has up to 9 layers (typically 4), whose fibres run in different directions, very much like a high-pressure tyre.

CO - cortical layer

ME - Medial layer

BA - Basal zone

implications of cuticle
Implications of cuticle:

The fibres are inelastic, so preventing changes in body volume while permitting lateral undulations. This high internal pressure defines many aspects of the nematode’s life:

1: It means that their cross-section is always accurately circular

2: It accounts for the lack of circular muscle in the body wall.

3: It means that the pharynx has to double as a valve, preventing the gut contents from exploding, and that food has to be actively pumped down the pharyx into the gut.

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4: When defecating the animal simply opens its anus, and the resulting jet sqirts out at high speed. Ascaris in the lab squirts up to 60cm!

5: It means that most species are superficially very similar in external morphology.

6: Cilia are quite unable to pump against such pressure gradients, and have been lost in the phylum - all pumping action is muscular. Interestingly the sperm seem not to be ciliated, and move by amaeoboid action.

7: Most species are dioeceous - cross fertilisation is the norm, and when mating the male has to wrap tightly around the female otherwise she would explode upon penetration!

nematode eggs
Nematode eggs

80μm

Trichuris egg

Parallelling the tough cuticle, nematode eggs are also thick walled and highly resistant, allowing some to build up egg banks in heavily contaminated areas. This is a real problem both for the plant- and mammal-parasitic radiations.

The eggs are remarkably uniform in size c.50m diameter, with 7m whale parasites having eggs the same size as 1mm soil dwellers.

(There is one obscure exception, a 7mm nema from antartica which produces 1mm diameter eggs)

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The outer coating of the egg often has ornate proteinaceous features, of some taxonomic use.

Most Nemas produce eggs in prodigious quantities. A typical gut parasite releases 15,000 eggs per day. One such prolific producer the human hookworm Ancylostoma duodenale may shed eggs at this rate for its life of 5 - 15 years.

Ancylostoma duodenale and eggs

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8: The cuticle’s inflexibility is a problem for growth, and is solved by the cuticle being shed at regular intervals (much like a snake shedding its skin).

This is accompanied by the release of fluid which built up between the old and new cuticles, which is one of the few things nematodes release to provoke a strong immune response.

There are 5 stages (separated by 4 moults), of which the 1st 4 are larval and the final is the sexually mature adult. It is common for 1 or 2 moults to take place in the egg before hatching.

senses
Senses

Nematodes have rather limited sensory capabilities, probably reflecting their relative impregnability. The thick cuticle is also a problem, in that nerves have to traverse the cuticle without weakening it unduly.

They have some chemosensors in the head and anal regions, some specialised sexual sensory organs, and a few species have occelli for light detection. (The presence of these sensory organs is of taxonomic significance, with the main division within the phylum being into 2 classes based on the occurrence of caudal sensory pits called phasmids.)

eutely
Eutely

A curiosity of the phylum is its economy with cell numbers. After the earliest sytages of embryogenesis, cell number is fixed, and all subsequent growth occurs by cell expansion. This state is called Eutely. (What does this mean for the ability to repair damaged tissues?)

The development is highly deterministic, with each cell in the body uniquely identifiable. This has made nematodes useful for studies of development, notably Caenorhabditis elegans whose entire genome has been mapped and whose development is well documented.

feeding
Feeding

There is also a wide range of feeding habits, despite the constraint that all food must be pumped in as a liquid or very fine suspension.

The commonest feeding habit for free living species is bacterivory, ingested as a suspension (such as in soil solution).

Some species have evolved tough plates around their mouths which act like jaws, and allow the nematode to act as a predator. Prey is punctured and the contents sucked out under the muscular action of the pharynx.

Other species are phytophagous or mycophagous. They puncture the plant / fungal cell with a hypodermic-like stylet on the anterior end, and suck out juices.

Xiphynema + stylet

slide14
Gut

The gut is a single-celled tube, with no cilia or muscles. Its transit time is very short, around 3 minutes, with the animals defecating continuously as fast as is compatible with their hydrostatic pressure.

It is thought that this is too fast for much enzymic action, and that they simply absorb useful nutrients without engaging in digestion per se.

respiration
Respiration

These animals are encased in a thick cuticle, and have no differentiated gills or other O2 exchange surface. How do they get their O2?

They don’t! Many nematodes lack crucial enzymes in the Krebs cycle, showing that their metabolism has to function without oxygen. This is not fatal - it just means that they are inefficient in extracting energy from foodstuffs.

slide16

I wrote this page a few years ago, in the hope of inspiring undergraduates to think about the constraints imposed by ecdysis..

Similarities to arthropods..

No-one suggests that nematodes have any close evolutionary connection to arthropods, but both have evolved with a thick cuticle between them and the outside world, and some convergent traits can be seen. Both moult the cuticle (obvious and unavoidable), only becoming sexually mature after the final moult (not so obvious). Both have specialised thinnings in the cuticle for the sense organs, but the active and highly mobile arthropods have evolved far more sensory organs + gas exchange surfaces. Both have lost cilia in the gut and the sperm (odd - so have higher plants). Any other parallels?

Since then, DNA analysis of highly conserved sequences has led to the creation of a superphylum ecdysozoa, containing arthropods and nematodes.

parasitic forms
Parasitic forms

The huge majority of nematodes are harmless eaters of bacteria and fungi, in muds and soils. This should be remembered as we explore the parasitic forms, because these tend to make the bigger impression and give the whole phylum a bad reputation.

The phylum has produced many parasitic radiations, because the fundamental design is pre-adapted to endo parasitism.

The extent to which they are pre-adapted to parasitism is reflected in the observation that parasitic species show almost no modification of body form, in sharp contrast to most invertebrates (ie flukes in mammals).

slide18

1:The thick body wall is an excellent protection against chemical or immune attack, allowing them to survive gut acids or antibody attack. (Antibodies certainly do bind to nematode cuticle, but can’t puncture it. Imagine throwing magnets at a suit of armour!)

2: The vast numbers of resistant eggs allow dispersal in time and space, maximising the chance of infecting a new host.

3: The microphagous habit pre-adapts to a gut content / body fluid diet.

4: The body design works well at small body size, which is advantageous for most parasitic lifestyles.

slide19

The basic lifestyle involves sexual fertilisation, release of eggs whch hatch into larval nematodes, identical in shape form and cell number to their parents. These undergo 4 moults to attain adult size. Parasitic species follow this pattern exactly, but still have a diversity of life styles.

Plant parasites

Fungal feeders

Animal parasites

plant parasites
Plant parasites

Many nemas have evolved to parasitise plants, usually by attacking their roots. Some species have evolved needle-like mouthparts to suck sap. These damage the plant directly, and also are implicated in transmitting plant viruses. They live outside the root so are known as ectoparasitic forms; Typical species: Xiphynema, Longidorus. Apart from feeding these have lifestyles like free-living soil species.

slide21

Endoparasitic spp invade the hosts’ tissues, often with high levels of specificity.

The potato root eel worm Heterodera rostochiensis is an extreme case, a true cyst-forming nema.

2nd stage larvae are mobile in the soil, and attack potato roots. They invade the root and feed on cortical cells. Females become fastened to the root while males retain some mobility, to find and mate with the stationary females. The female becomes a sac of eggs, fastened to the root, the potato cyst. Its eggs remain viable for years and are a serious agricultural pest.

invertebrate parasites
Invertebrate parasites

Some (?the majority?) of nematode spp are invertebrate parasites. These are mainly of interest as biological control agents.

Mermis spp are active against grasshopppers and have been studied to control locusts (so far not on a serious field scale).

One nema Phasmarhabditis hermafroditais marketed as a slug control agent, though the field trials in the UK have been rather patchy so far. 300,000 m-2 every 14 days!

human parasites the benefits
Human parasites – the benefits!

Before you get too nauseated by what nematodes do in human bodies, remember these points:

1: All you ancestors for millennia carried these worms mush of their lives; we are co-evolved, and our immune system is evolved to attack worms on a daily basis.

2: There is compelling experimental evidence that having some nematodes in your gut exerts a helpful dampening down of the immune system, especially useful against auto-immune diseases. If I had an auto-immune bowel disease I would certainly make a point of getting a nematode infection! They may dampen asthma too.

mammalian parasites
Mammalian parasites

If you think this is revolting, try doing a google image search for Ascaris. If you have a strong stomach.

A typical example of a mammalian parasitic nema is Ascaris lumbricoides the human roundworm, which is up to 20cm long. (A closely related species is found in pigs).

This was recorded in chinese records 4700 years ago (where it was correctly stated to be caused by eating eggs off raw vegetables) and egyptian medical records 3000 years BP.

Aristotle stated this species arose spontaneously in the gut, thereby setting back biology by 2000 years (!).

the circulatory sojourn
The circulatory sojourn

The first two larval stages take place within the egg before hatching. The egg matures after being excreted in faeces, and will not hatch unless eaten by a new host.

The third stage emerges in the alkaline conditions of the mid gut, and burrows through the gut wall. It swims in the blood until the right side of the heart, thence to the lungs, where they penetrate the lung wall, are coughed up with mucus and re-swallowed to become adults. This lung passage was only discovered in 1915.

slide26

Ascaris eggs pass out with faeces and stay viable for decades - old asylums often have heavy infestations. Nowadays one pill sorts it out (“Ovex”).

Although basically benign, this species sometimes kills humans by blocking your intestine with hundreds (that emerge from anus, mouth and nose in heavy infections). The mass of nemas is so dense that some 20cm adults penetrate the gut wall and wander around the body cavity.

A few people become intensely allergic to nematodes - there are stories of technicians who could not enter a lab where Ascaris was being dissected without starting an allergic reaction. If such a person gets a gut infection they will probably experience anaphylactic shock when moulting fluids are released.

slide27

Many other parasitic species (such as the facultative parasite Strongyloides) have this curious lung-penetration sequence for reasons that are not understood, while other gut parasitic species do not. The technical term is a circulatory sojourn, and causes minor damage both to the lung wall and to the gut.

This is dwarfed by the damage caused by a misfunctioning of this system. If the infestation is high, or species-host adaptation is poor, some larvae fail to penetrate the lung capillaries but iunstead return to the heart (left side) and are pumped on to the rest of the body. The larvae then penetrate capillaries in body organs, causing mechanical damage and scarring. This is known as visceral larva migrans, and can cause serious or fatal damage to the host.

Toxocara canis – from dog faeces to human nervous systems; children have suffered eye and CNS damage.

enterobius vermicularis
Enterobius vermicularis

Most of you here will have been infected with nematodes, at least some of you will have them in your guts today. Luckily the commonest nematode in western European humans is tiny and harmless - the pinworm Enterobius vermicularis. The females emerge from your large colon an hour after bedtime to lay eggs around the anus. (You almost never see the males, who stay inside the colon as long as they live). This irritates the skin, so you scratch and get the sticky eggs on your fingers. These go into your mouth, and being sticky adhere to door handles (especially toilet doors), bedclothes, mug handles etc.

slide29

Nematode eggs are very tough and stay viable for months or years. Enterobius often affects hotel maids who breathe the eggs in as dust, and is an occupational hazard in the laundry trade. Kids who are restless a while after bedtime should be checked for Enterobius. The worst it usually causes is to enter the vagina, where it causes really nasty itching that persists long after the infection is cleared up.

In Holland after the 2nd WW 98% of the population was infected with Enterobius - this was surveyed by a simple technique in which cellotape is left stuck across the anus all night, and its surgface subsequently examined for eggs. Luckily Enterobiusdoes no harm and is easily cured with a pill from chemists.

hookworms
Hookworms

Two genera of nematodes cause serious human debiliation: these are the hookworms, Ancylostoma duodenale (the old world hookworm) and Necator americana (new world hookworm). Their larvae live in soil for the 1st 2 instars as harmless bacteria-eaters.

The third instar enters human blood (by being eaten or by forcing its way into the skin, usually up a hair follicle or wound), then is coughed up from the lungs and enters the gut.

slide31

Unlike Ascaris or Enterobius, these species use their tough toothed anterior ends to browse on gut villi, causing serious localised damage. Each worm causes losses of about 0.5ml blood per day, so a typical infection of 100 worms leads to 50ml blood loss per day. This causes weakness, anaemia and general debilitude, with mental retardation developing after years of infection.

These species are commonest among communities where people walk barefoot in faecally contaminated soil - the dwellings of the very poor. Not just the third world; hookworm was an endemic problem in the poor blacks of southern states in the USA. The ill health resulting only increases poverty and has been seen as a cycle of deprivation. When the hookworm lifestyle was elucidated it was hailed as “the worm that causes poverty”.

(Needless to say, curing hookworm with piperizine and proper sanitation has not ended poverty...)

slide32

The Guinea worm Dracunculus medinensis is one of the more notable human parasites, known since antiquity. It is thought to be the old testament ‘fiery serpents’ which affected the israelites. It has 2 hosts; a freshwater crustacean (Cyclops etc), and man. The adult female is unusually large, c. 40cm and lives below the host’s skin. Eggs may be produced parthenogenetically as males seem to be scarce.

slide33

The eggs hatch in utero and undergo a moult. When ready the female causes a boil to arise on the hosts skin, and sticks a portion of her uterus (prolapsed) out of the ulcerated hole. When she senses that the host is bathing (by a sudden fall in temperature) she ejects larvae by rupturing her uterus.

The larvae cannot develop further unless eaten by a crustacean (copepod), where they hatch and moult twice. Typically one copepod can support one larva - multiple infections will kill the crustacean.

If the crustacean is drunk by a human, the nemas emerges into the gut lumen, then forces its way into the blood stream. The female alone punctures the hosts skin, to repeat the cycle. The interval from drinking the infective Cyclops to release of new larvae is about 12 months.

slide34

Note the thread dangling out of the open wound. This is the female nematode, whose prolapsed ovary sheds filaria on immersion into cold water.

slide35

The problem is that this parasite maintains an open wound, which is a likely cause of infection for the host. Her body can be seen running below the hosts skin for many cm, but is too delicate to be pulled out. If she is torn, her body will rot under the hosts skin and septicemia is certain (probably fatal). The solution is to pull her out very slowly, winding her around a stick.

This rather ghastly procedure is ancient, and thought to be the origin of the aescepulean snake wound around a stick which is the symbol of medical practice.

slide36

Biodiversity paradox:

We can eliminate Dracunculus infection in humans, and it is on the WHO’s target list (possibly after polio). In fact it was a UNICEF goal for children #25 to eliminate it by 2000 (failed). It’s easy to eliminate – educate people to recognise the boils, not to expose these to water, to drink filtered water (not even boiled – a strainer will do to remove the crustaceans).

Then we lose a part of human history – there are other Dracunculus species: D. insignis attacks a variety of aquatic predatory mammals (otter, racoon, fisher, mink). But D. medinensis is human-endemic, and is said to have given us the icon of medicine. (I’m not sure that story is true, but the association is still noteworthy.)

aesculapian snake

slide37

Trichinella spiralis is a gut parasite of omnivores and carnivores. It causes incurable muscle damage. Adults mate in the hosts gut, and the eggs hatch rapidly producing larvae which penetrate the gut wall. Unlike many nemas these larvae attack muscle cells (with a lancet and cytolytic enzymes) wherein they grow and moult 3 times. These stay encysted in the muscle, waiting for the muscle to be eaten. When eaten, the larvae excyst, moult and infect a new host.

This is basically a parasite of rats (which are cannibalistic), but infects pigs when pigs eat a rat. The problem for humans is not the adults, but the encysted larvae in our muscles. They degrade muscle performance (there being selection pressure to weaken the intermediate host), and are presently incurable.

Although Trichinella encephalitis is rare, it is life threatening.

wucheria
Wucheria

The one I really wouldn’t want to get is Wucheria bankroftii, causing filariasis = elephantiasis. This nematode is minute (<0.1mm) and lives in the circulating blood of its human host. The larvae are small enough to be sucked up by mosquitos. This allows transmission to a new host.

Inside the host each individual worm does minimal harm, but en masse the numbers become large enough to clog up lymph ducts. This prevent fluids draining out of tissues, so the tissues expand, slowly but inexorable. Filariasis in the leg can make 1 leg swell to 40cm diameter or more, puffy soft flesh.

The same condition causes hideous facial swelling, and the worst is the scrotal infection, where the unfortunate male has to go around with his testes supported by a wheelbarrow. We can now kill the infection, but not repair the damage caused by a long-standing swelling.