Labyrinthulomycota: navigating the maze

Three years ago when I started a degree in human biology, I had no idea that a year later I’d be studying parasitic rust fungi at the Royal Botanic Gardens. The following year I somehow found my way into a bacteriology lab, studying membrane fluidity in hydrocarbon-degrading bacteria. Which brings me to my current research project in, of all places, a shellfish immunology lab. Despite having utterly no idea how I ended up here, I’m very glad I did. My task is to investigate the bivalve immune response to a pathogenic species of thraustochytrid.

In light of the fact thraustochytrids are not exactly David Attenborough material (though I wish they were!) I probably ought to start with a straightforward definition – they are marine, apochloriotic, straminopile protists.  Okay, not that straightforward. Essentially, thraustochytrids are single-celled, fungus-like organisms that live in the ocean, mainly as decomposers, mutualists, or parasites. They belong to a curious group, the Labyrinthulomycota, who owe their mycological-sounding name to the fact they were historically considered as marine fungi. But fungi they are not.

Members of this group, including the species I’m studying, all have one weird thing in common: a special organelle called the bothrostome. Labyrinthulomycetes use this machinery to weave an ectoplasmic net, which they use as a sort of superhighway, gliding along at 150μm per minute, deploying hydrolytic enzymes to break down food. They can also use their ectoplasmic net to cling to various surfaces, such as rocks, shellfish, glass and aluminium. This footage, filmed by German mycologists in 1966, captures L. cynocystis putting on a dazzling shape-shifting display. Filmed in 16mm under phase contrast, the cells almost resemble a bustling, night-time metropolis.

This is all quite weird and wonderful – but why study Labyrinthulomycetes? As with their morphological showmanship, when it comes to ecological and biotechnological value, they do not disappoint. With ever-growing concerns regarding global warming, energy security and oil prices, thraustochytrids have sparked a great deal of interest as an alternative feedstock for biofuel production. This is owed to the fact that they produce copious amounts of lipids, including omega-3 long chain polyunsaturated fatty acids (PUFAs). Using hydroprocessing techniques, these lipids can be converted to biodiesel. Additionally, with everybody from health authorities to celebrity chefs ordering us to swap unhealthy fats for polyunsaturated alternatives, it is unsurprising that thraustochytrids have also caught the attention of the nutraceutical industry, as a novel candidate for omega-3 production.

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Above: Micrographs from my recent experiments: thraustochytrid 50A undergoing cell division (left). What looks like Mickey Mouse ears on the right is actually a grain of pine pollen – the small spherical cells surrounding it are unidentified thraustochyrids, isolated from the blue mussel (M. edulis) using pollen-bating.

Regrettably, thraustochytrids also have a dark side: they can be parasites. In 1976, a young marine biologist at St. Andrews University noticed something unsettling in her aquarium. The octopuses she was studying at the time began acting strangely – violently shaking their tentacles and continually running their arms over their body and head. When she looked closely at the sickly animals, most of which promptly died, she found ulcerative lesions all over their body and arms. The invisible presence responsible for this cephalopod carnage turned out, of course, to be a thraustocytrid. Not to be outdone, the researcher took samples from the lesions of infected animals, and examined them under the microscope. Noticing that they resembled the Labyrinthula, she then proceeded to bring them into pure culture, using an old-school mycological technique known as pollen-baiting. It is this species, yet to be formally identified but for the time being tentatively called ’50A’ (above, left) which I am currently researching at the Heriot-Watt Centre for Marine Biodiversity.

E. cirrhosa is not the only animal to fall victim to pathogenic thraustochytrids. The hard clam, or Quahog, is a bivalve mollusc native to the eastern shores of North America. Quahogs are highly prized as a delicacy, especially in Rhode Island – still known to some as ‘Quahog country’. Their shells were even used as currency in 17th century New England. More recently, however, tough times have befallen the hard clam, as a thraustochytrid parasite – ominously named QPX (Quahog Parasite Unknown) – has devastated clam stocks in Massachusetts, New Jersey and Virginia. Once a clam is infected with QPX, it undergoes a massive inflammatory response, ultimately bringing the individual to an untimely demise (in the absence of predators, clams can live for up to 60 years). Mass mortality often ensues, with losses of 80-95% reported in some areas. For growers, the only available management strategies are vigilance and keeping nets clean to avoid transmission.

rusts

Above: Poplar rust spores (left) collected from a park in Sighthill during my fieldwork with RBGE. A 180 year old sample from the herbarium (right). The pustules on the underside of the Sorbus leaf are a sign of Gymnosporangium sp. infection. Rusts are highly specialised fungal parasites, notorious within agriculture and horticulture circles for their canny ability to cycle between two unrelated hosts, leaving destruction in their midst.

QPX remains a mysterious disease, but developments in high-throughput sequencing technology have spurred several investigations into its molecular makeup. Unfortunately, a lack of gene bank information regarding similar thraustochytrids means that much of this work feels a little like stabbing around in the dark.

Which brings me to an important point – we need to study the obscure stuff.

Let me explain: one could be forgiven for thinking that thraustochytrids don’t amount to much; most biologists haven’t heard of them let alone could pronounce their name (admittedly I was one of these people up until a few months ago). Thanks to some great science communication, however, parasites (I’m thinking zombie roaches and Toxoplasma) have been making quite a name for themselves recently. As an aspiring parasitologist this pleases me to no end, but on some level, work is needed to elevate little-studied organisms such as the Labyrinthulomycetes or amazing rust fungi to a status beyond mere curiosity value. Obligations under the Convention on Biodiversity require the study of all organisms, obscure parasites included, if conservation is to be stepped up in a time of massive environmental change.

When I started out at university I had high hopes of becoming the sort of biologist who works tirelessly in a heroic struggle to eradicate some human disease. I’m not ruling out a return to human health, but for now I’m happy where I am – in a shellfish immunology lab. One of the best and most unexpected things about my undergraduate degree has been the limitless array of wonderful organisms to study. From human health and plant pathology, to marine bacteriology and shellfish immunology, biology for me has been an ever-expanding maze; one I’m happy to remain thoroughly lost in.

James Iremonger (c) 2015

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