Polypocephalus sp.

Today's parasite might be thought of as an "aquatic Toxoplasma" in that it also induces behavioral changes in its hosts. Polypocephalus is a genus of tapeworms that infects both shrimp (Litopenaeus setiferus) and then likely rays such as the Atlantic stingray, (Dasyatis sabina). The larvae of the cestode invade the neural tissue of the shrimp hosts, particularly in the abdominal ganglia. Studies recently showed that the more larval tapeworms a shrimp had, the more time these hosts spent walking on the substrate, as opposed to sitting still or swimming. Although the authors had predicted that they would see an increase in swimming behavior because that might expose them to predation more readily, perhaps just the increased activity in general is enough to promote transmission. Nonetheless, this was an exciting insight into a potentially new system for studying parasite manipulation of their hosts.

Source: Carreon, N., Z. Faulkes, and B. L. Fredensborg. 2011. Polypocephalus sp. infects the nervous system and increases activity of commercially harvested shrimp. Journal of Parasitology 97:755-759

Image from figure of that paper.

Bursaphelenchus xylophilus

Today's parasite is the nematode Bursaphelenchus xylophilus, a well-known tree-killer responsible for the devastating plant disease known as pine wilt. Originating in North America, it has since been spread over much of Asia, and has recently been introduced to Europe. This nematode is transported by longhorn beetles known as "pine sawyers", and gain initial access to the tree through the feeding wound created by that insect. So the arrival of a B. xylophilus-laden beetle pretty much amounts to a death sentence for a pine tree. While pine trees in North America have coevolved with B. xylophilus and developed resistance or tolerance for the parasite, it has caused widespread wilting and death to the pine trees of Japan. So how can such a tiny worm bring down an entire pine forest?

For B. xylophilus, or any other plant parasites for that matter, a tree is a formidable fortress - protected by walls and scaffolding of tough cellulose, and canals of deadly resin. Plant cell wall presents the main barrier to any plant parasites - it is a tough material to break down, and most animals are incapable of doing so without the aid of symbiotic microbes. In addition, the vascular tissue of many coniferous plants like pine are saturated with resin - a thick, sticky cocktail of aromatic chemicals (from which we derive many useful substances including solvents, varnishes, adhesive and perfume) which would overwhelm and kill most invaders. Yet none of those defenses seem to deter B. xylophilus - not only can it break through the thick cellulose barrier of the pine tree, it actually lives within the resin canals of its host, which is practically the most lethal place within the tree. It would be akin to living in a moat of toxic tar.

A recent study published in PLoS Pathogens on the genome of B. xylophilus offers vital clues to how this nematode exploits its pine tree host. One of the most important enzymes for plant exploitation is cellulase - it is used to break down cellulose structures and allow potential parasites to enter and navigate through the host. Bursaphelenchus xylophilus is able to produce a unique combination of 34 enzymes for breaking down cellulose and carries a diverse suite of genes for producing enzymes that detoxify the aromatic compounds found in resin. So how did this tree killer acquire the necessary molecular machinery to invade and disarm its host?

The wide range of detoxifying genes in the B. xylophilus genome appear to be multiple duplication of pre-existing genes which are also found in other nematodes, such as the well-known standard lab worm Caenorhabditis elegans - B. xylophilus just happen to have more of copies of those genes to cope with the wider array of toxins it encounters. However, the cellulase genes have a much more unusual origin. Out of the 34 cellulase enzymes produced by B. xylophilus, 11 of those enzymes are not found in any other nematode, but are most similar to those produced by fungi. So how does a nematode end up producing fungal enzymes?

The answer might be through horizontal gene transfer (HGT). The closest living relatives of B. xylophilus are fungi-eating worms which are transported by beetles to dead and dying trees. Once they reach their destination, they disembark from their beetle vectors and feed on the fungi which have colonised the dead trees. In a case of you are what you eat, the ancestors of B. xylophilus appeared to have incorporated a whole suite of useful genes from their food, allowing them to bypass the process of feeding on fungi which are growing on dead trees and just go straight to breaking down live plant tissue.

Image from figure of the paper.

Reference:

Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N, et al. (2011) Genomic Insights into the Origin of Parasitism in the Emerging Plant Pathogen Bursaphelenchus xylophilus. PLoS Pathog 7(9): e1002219. doi:10.1371/journal.ppat.1002219

Nicothoë astaci

The parasite we are featuring today is Nicothoë astaci, the "lobster louse." Despite its name, it is not a "louse" (true lice are insects) as such, but rather a copepod (a type of crustacean), just like the salmon lice we have previously featured on this blog. But whereas salmon lice are well-studied due to their economic impact on salmonid fisheries (especially on farmed fishes), far less is know about the lobster louse. Despite having been recorded on the European lobster (Homarus gammarus) since the 1950s, to this day there is very little known about this parasite, including the type of pathology it causes, its complete life-cycle, or even what the male of the species looks like (parasitic copepods often have cryptic or dwarf males which are very elusive).

The paper we are looking at today is taking the first step to rectifying that situation. The photo (from the paper itself) depicts larval stages of N. astraci, with the arrows indicating the oral cone,the structure this parasite uses (along with its front pairs of legs) to attach itself to the host's gill filament and feed on its blood. While the larval stage looks like a rather ordinary copepod, as it matures into an adult, it morphs into what looks like a miniature boomerang with a pair of stretched out "wings" on either side, and a pair of bulbous egg sacs dangling from its rear end. The attachment and feeding activity of the lobster louse can cause pronounced physical damage to the lobster's gill filaments.

As with any kind of infection, you would expect to see some kind of cellular response. While the innate immune systems of invertebrates like lobsters are not as sophisticated as the adaptive immune system of vertebrate animals such as ourselves, they can present a formidable challenge to any would-be intruder (to see an example of what the cellular defence of a crustacean can do to a parasite, click here). Basically, the crustacean's equivalent of blood cells wrap themselves around the parasite or pathogen and initiate the process of melanization, where the intruder becomes entombed in a hardened capsule of melanin (the pigment which determines our skin colour). The researcher did find signs of melanization and other cellular disruption throughout the gills of infected lobsters, but none of it was near the lobster louse's attachment point.

So the lobster's immune system recognizes the presence of an intruder, but is unable to pinpoint and focus its wrath on the parasite. The authors of this paper suggest that this indicates the lobster louse is able to somehow interfere with the lobster's defensive mechanism so that it can blood-feed in peace. The mechanism through which the lobster louse disrupts this particular aspect of host physiology is yet to be uncovered, along with much of the parasite's ecology and life-cycle. Hopefully, with further research on this host-parasite system, this situation will change in the future.

Image from the paper.

Reference:

Wootton EC, Pope EC, Vogan CL, Roberts EC, Davies CE, Rowley AF. (2011) Morphology and pathology of the ectoparasitic copepod, Nicothoë astaci ('lobster louse') in the European lobster, Homarus gammarus. Parasitology 138:1285-1295.

Maritrema subdolum

This is a story about two little crustaceans and a parasitic fluke. Corophium volutator and Corophium arenarium are amphipods that make a living tunneling in the mudflats on the coast of the Danish Wadden Sea. They are also host to many species of parasitic flukes, and one of them is the parasite we are featuring today - Maritrema subdolum. Last year, we featured a related species from New Zealand - M. novaezealandensis - and much like its Kiwi cousin, M. subdolum is the bane of the local crustacean population. However, M. subdolum does not affect all of its crustacean hosts equally and this has some important ecological consequences.

Out on the Danish mudflats, C. volutator is king. Of the two Corophium species, it is the stronger competitor, reaching much higher abundances and generally making life difficult for C. arenarium. But along comes M. subdolum, which evens out the playing field. Living alongside those little crustaceans are mud snails, and during early spring they can become extremely abundant, with over 25000 snails per square metre. By summer, almost half of those snails are infected with M. subdolum, which turn them into little parasite factories, each cloning a massive reserve of parasite larval stages call cercariae that are then unleashed into the environment to infect the amphipods. The main trigger for releasing these cercariae is high temperature, and during 1990 there was a bout of unusually high temperature during summer that has been linked to North Atlantic Oscillation (NAO), a phenomenon that plays a major role in determining climatic conditions in the northern hemisphere.

All of this combined into a perfect storm that devastated the C. volutator population. Triggered by high temperature, all the infected snails released their payload of parasites into the surrounding waters. Each infected snail can release hundreds of cercariae, and with thousands of snails per square metre, the shallow waters of the mudflats turned into a seething parasite soup. To the amphipod, this amounted to being in a shooting range, as each cercaria is armed with glands of digestive enzymes and a scalpel-like organ call a stylet with that they use to puncture the amphipod's exoskeleton. For many C. volutator, the outcome of being attacked by a swarm of these little horrors was terminal, and this resulted in a dramatic decline in their population. However, for some reason we still don't know, the C. arenarium population was able to weather the M. subdolum storm unscathed, either because they tolerated the parasite swarm, or because they were simply not the preferred target. Either way, with the collapse of the C. volutator population, in the next season, C. arenarium was able to succeed them and become the dominant amphipod species on the Danish mudflat.

And this dramatic ecological change was ultimately brought about by a little parasite.

Photo by Kim Mouritsen

Reference:

Larsen, M.H., Jensen, K.T. and Mouritsen, K.M. (2011) Climate influences parasite-mediated competitive release. Parasitology 138: 1436-1441

Metarhizium acridum

The locust in the photo is covered in a fine layer of green mold - that is because it was killed by the parasite we're featuring today, Metarhizium acridum. Metarhizium acridum is a pathogenic fungus which specifically infects and kills grasshoppers, locust and other insects in the Orthoptera order. Because of the pest status of some orthopterans (think locust plagues), M. acridum is mass-produced as type of environmentally-friendly, biological alternative to most insecticide. But while M. acridum only targets locust and grasshoppers, its close relative, M. robertsii, is far less picky, capable of infecting hundreds of different insect species.

So why is M. acridum so picky while its close relative is so indiscriminate? Amazingly, it appears to come down to a single gene call Mest1 - a gene present in M. robertsii, but is absent in M. acridum. To find out the function of this gene, a group of researchers in China created a mutant M. robertsii strain which has a non-functioning copy of Mest1. This mutant lost its ability to infect most insects - except grasshoppers and locusts - which happens to be the speciality of M. acridium. In parallel, the researchers also inserted functional copies of Mest1 into M. acridum. The insertion of this single gene allowed M. acridium to infect a wider range of insects.

What is so special about Mest1? In M. robertsii, Mest1 is expressed during spore germination, and plays an important role in initiating the infection process. Mest1 expression can be triggered by a range of stimuli including nutrient poor conditions or contact with insect cuticle. Metarhizium acridium has other genes playing the role of Mest1, but they are triggered by substances which are present only in the waxy coating of grasshoppers and locusts. So if its spores land on other insects such as caterpillars which have a different type of coating, M. acridum fails to germinate because the appropriate stimuli are absent. Thus, the insertion of Mest1 into M. acridium allows the fungus to bypass those usual stimuli and begin germinating under a wider range of conditions

Host specificity is one of the central question in the evolutionary biology of parasitic organisms. In this case, we can see how a single gene can changed this otherwise specialist pathogen into a broad-spectrum generalist.

Image from the Wikipedia.

Wang S, Fang W, Wang C, St. Leger RJ (2011) Insertion of an Esterase Gene into a Specific Locust Pathogen (Metarhizium acridum) Enables It to Infect Caterpillars. PLoS Pathog 7(6): e1002097. doi:10.1371/journal.ppat.1002097

Parvilucifera sinerae

Phytoplankton are microscopic single-celled "plants" which float in the upper surfaces of the ocean, and their photosynthetic action is responsible for generating most of the oxygen in our atmosphere. While you might think that something so tiny would not be host to anything, there are in fact a myriad array of viruses, bacteria, and flagellate organisms that infect and exploit phytoplankton, and the parasite for today is one of them. Parvilucifera sinerae is a single-celled, flagellated organism which infects dinoflagellate algae such as Alexandrium minutum. The photo shows an infected A. minutum cell. While earlier in this post we extolled the virtue of phytoplankton, dinoflagellate algae are also known to be responsible for harmful algal bloom events such as "Red Tides", so there is a lot of interest in their ecology and the factors that can influence their likelihood of blooming.

For P. sinerae, infecting its host is not an easy task - not only does it have to find a swarm of its tiny host in the vast ocean, it also needs to make contact and accomplish what amounts to a cellular heist - the parasite needs to break through the protective shell of the alga in order to steal its valuable content. As you can imagine, during such an intense operation, being jostled around will probably throw you off your game. And indeed that is what a group of scientists in Spain have found. It appears that even a slight turbulence is enough to reduce the infection success of P. sinerae and that it performs best under calm, still conditions. These researchers suggested that turbulence would erode the zone of chemical emission around the dinoflagellate, making them more difficult to detect. Turbulence would also shorten the period of time which P. sinerae are in constant contact with the host cell - which is a necessary precondition for the parasite to perform its little cellular heist.

While both P. sinerae and its host are tiny, their interactions can have far-reaching ecological consequences, and as explained earlier they are among the most important organisms on the planet. In addition, parasitic killers, such as today's parasite, have been suggested as a possible biological control for harmful algal blooms, but it is like that the effectiveness of any such control would be at the mercy of environmental factors such as small-scale marine turbulence.

Image from figure of the paper.

Reference:
Llaveria, G., Garcés, E., Ross, O.N., Figueroa, R.I., Sampedro, N. and Berdalet, E. (2010) Small-scale turbulence can reduce parasite infectivity to dinoflagellates. Marine Ecology Progress Series 412: 45-56.

Sphaeromyxa cannolii

We've met other myxozoan parasites before, including the very well-known causative agent of whirling disease in salmonid fishes, Myxobolus cerebralis. Today, meet a newly described species of myxozoan that was found infecting seahorses collected from the Gulf of Mexico. Not only was this the first such species described from this seahorse, but this is also the first time that any pathology attributable to a species in this genus has been recorded. The abundance of the parasites in the liver was observed to obstruct the bile ducts of the fish, which caused noticeable accumulation of bile in the diseased hosts. The intermediate hosts are presumed to be some kind of annelid worm, but remain unknown for this species. And in case you were wondering, yes, the species name for this parasite comes from the fact that it looks like a cannoli.

Image from the paper.

Reference: Sears, B.F., P. Anderson, and E.C. Greiner. 2011. A new species of myxosporean (Sphaeromyxidae), a parasite of lined seahorses, Hippocampus erectus, from the Gulf of Mexico. Journal of Parasitology 97:713-716.

Cardicola forsteri

Today's parasite is a blood fluke that has been turning up in tuna ranches in South Australia. The blood fluke lives the tuna's circulatory system, and lays eggs that can become lodged in the fish's gills or other organs such the heart, and cause significant lesions in those tissues. This is obviously of great concern to the tuna ranchers, so they set out to find a way of alleviating their fish from infection.

Being a trematode, Cardicola fosteri must have an invertebrate host that is the source infection for the tuna. In their search for the first host of C. forsteri, researchers undertook a a truly heroic effort - sampling over 9000 (!) invertebrates, including all kinds of bivalves, snails, and polychaete worms from the pontoons on the tuna ranch and nearby areas, then meticulously dissected and examined every single one of them for parasitic infections. Those who have been following this blog would know that trematodes usually have a mollusc host in which they undergo asexual multiplication - usually a snail, but C. forsteri is very unusual - it turns out that it uses a polychaete worm, specifically tube-dwelling terebellids - also known as spaghetti worms - for asexual multiplication. Infected worms were packed with hundreds of sac-like sporocysts which continuously churn out the free-living cercarial stages that go on to infect the tuna.

The researchers then used specific sections of the DNA obtained from the parasites to match up the sac-like sporocyst stage in the worms with the adult stage in the tuna, and they were able to confirm that the blood flukes in the tuna were indeed originating from those infected tube-dwelling worms. As those sedentary worms usually live on the seafloor, researchers recommended that simply by moving them to deeper waters, the tuna would be infected by far fewer blood flukes. This study shows how understanding the ecology and life-cycle of a parasite can help us take straightforward measures that can mitigate their impact.

Photo by Robert Adlard

Reference:
Cribb TH, Adlard RD, Hayward CJ, Bott NJ, Ellis D, Evans D, Nowak BF. (2011) The life cycle of Cardicola forsteri (Trematoda: Aporocotylidae), a pathogen of ranched southern bluefin tuna, Thunnus maccoyii. International Journal for Parasitology 41:861-70.

Skrjabinoptera phrynosoma

Life isn't easy as a parasite with a complex life-cycle. In order to grow up and reproduce, you often need to make your way through the bodies of at least two very different host animals - a very haphazard process that depends largely on timing and luck. In the case of today's parasite - a nematode worm called Skrjabinoptera phrynosoma - it has to make its way between a lizard and an ant. The adult S. phrynosoma lives inside the stomach of the desert horned lizard Phrynosoma platyrhinos. However, when the female becomes filled with mature eggs, she migrates to the lizard's cloaca (a nice, technical way of describing a lizard's butt).

Unlike most parasitic nematodes, which often lay eggs that are cast out of their host and left exposed to the elements, S. phrynosoma is a very maternal parasite - in a slightly morbid way. The female S. phrynosoma makes the ultimate sacrifice by casting her egg-filled body out of the lizard via the host's feces. She will die outside of the host - but in addition to protecting her eggs by doing so, it is also her strategy for helping her eggs reach the next host. For some reason, ants find the shriveled, egg-filled cadavers of female S. phrynosoma to be a tasty treat, a meal fit to feed to their brood of growing ant larvae - which then become infected with the parasite's own larvae. The life-cycle is complete when the infected larvae mature into workers, emerge from the colony, and become lizard food - horned lizards are specialists on ants.

Researchers at Georgia Southern University discovered that to ensure that this sequence of events occurs, S. phrynosoma has evolved to synchronise its life-cycle with the seasonal behaviour of both its lizard and ant hosts. They found that the number of egg-filled females (all ready to evacuate) reach peak abundance during the middle of the lizard's mating season. This is also the period when there are the greatest number of ants out busily foraging and when the colonies are packed to capacity with broods of growing ant larvae. By timing its life-cycle in such a manner, S. phrynosoma ensures that when next season rolls around, when those broods of larvae are ready to emerge as a new generation of workers ants, they will be doing so pre-infected with nematodes and just in time to welcome the hungry lizards coming out of hibernation.

Reference:
Hilsing, K.C., Anderson, R.A. and Nayduch, D. (2011) Seasonal dynamics of Skrjabinoptera phrynosoma (Nematoda) infection in horned lizards from the Alvord Basin: temporal components of a unique life-cycle. Journal of Parasitology 97: 559-564.

Caenorhabditis briggsae (KT0001)

Today's parasite is in the same genus as the famous and well-studied model lab nematode worm Caenorhabditis elegans. Caenorhabditis briggsae is a relative of C. elegans and is often used in comparative studies with its more famous counterpart because many of the tools developed for C. elegans can also be used on C. briggsae. While C. elegans is the darling lab worm due to its usefulness in studying genetics and developmental biology, until very recently, very little is known about its natural ecology.

Worms in the genus Caenorhabditis are often associated with invertebrates, hitching a ride on them as a way of traveling between food sources, or even opportunistically feeding on their ride if it happens to drop dead for whatever reason. In a paper published last year, a group of researchers reported on a strain of C. briggsae (KT0001) from South Africa displaying an ability not previously known for any Caenorhabditis species - it is capable of infecting and killing wax moth larvae. This strain of C. briggsae was found to be in a symbiosis with the pathogenic bacteria Serratia which presumably allows C. briggsae (KT0001) to become a parasitic killer.

Furthermore, when the researchers tested 10 wild strains of Caenorhabditis species which had not previously displayed any ability to infect insects - including a strain of C. elegans - and cultured them with Serratia, all but one strain gained the ability to infect, kill, and reproduce in insects, including the famous C. elegans. It seems that Serratia gives Caenorhabditis a license to kill - upon forming a partnership with the bacteria, these worms turn from mere passengers into deadly killers.

Reference:
Abebe, E., Jumba, M., Bonner, K., Gray, V., Morris, K., Thomas, W.K. (2010) An entomopathogenic Caenorhabditis briggsae. Journal of Experimental Biology 213: 3223-3229.