Pseudoalteromonas luteoviolacea, showing off its surprisingly two-toned colonies in a laboratory culture dish. Image courtesy of Nicholas Shikuma

Like a steaming pile of lava or the soggy soil below a melting glacier, the freshly scrubbed hull of a ship is a magnet for new life. The first creatures to the party are microbes like Pseudoalteromonas luteoviolacea, bacteria named for their curious habit of coloring themselves both yellow and purple in lab dishes.

But the party is a problem, because P. luteoviolacea and microbes like them trigger a chain reaction that hairs hulls over all over again with barnacles, tube worms, and other pernicious encrusting life.

Whether you’re a 17th century privateer, a 20th century rum runner, or a 21st century sailor driving an aircraft carrier, this is bad news. That’s because this life is literally a drag and results in potential apprehension by the Royal Navy, the Feds, or, in millions of dollars of wasted fuel spent pushing these freeloaders through the water.

But what is most remarkable about P. luteoviolacea is not that it triggers growth that would make the Hair Club for Men jealous, but how, at least in the case of the ship-encrusting tubeworm Hydroides elegans: P. luteoviolacea builds bristling blossoms of injectable virus tails linked by intricate hexagonal nets that are somehow used by young tube worms to detect their landing site.

In this movie that shows a microscope zooming in and out through successive layers of a bacterial cell, a computer reconstruction is superimposed to help you see how the structure would look in 3D.

No one can yet fathom why they build and release these prickly flowers constructed from components apparently purloined from viruses that attack bacteria. These mystery structures are somehow used by marine tubeworms to sense when they have reached the promised land of a naked ship hull ripe for colonization, as well as to trigger their metamorphosis from drifting squibby larva to proper settled-down young tubeworm. The world of biology is full of strange evolutionary convolutions, but this, even by my standards, is bizarre.

Hydroides elegans is not one of those tube worms you’ve heard about — the giant ones with the lurid red bodies that grow around sexy hydrothermal vents billowing hella hot black smoke. Hydroides elegans is more of a blue-collar tube worm.

Image courtesy of Brian Nedved

For scale, here they are posing next to George Washington’s head.

Image courtesy of Brian Nedved

It lives its life as other tube worms do, beginning life as a drifting larva

Image courtesy of Brian Nedved

that ultimately metamorphoses into a young tubeworm,

Image courtesy of Brian Nedved

settles down, grows a tube, and sticks its feathery feeding tentacles into the water to grab whatever delicious detritus the ocean might drag its way. When it decides to get in the family way, it dutifully releases its eggs or sperm (as appropriate) to the water, and goes on about its business until the reaper cometh.

Though small and humble, they are still quite beautiful. If you cruelly yank one out of its tube, it looks like this:

Image courtesy of Brian Nedved

But how does a young larva make the ultimate commitment: where to glue its tube? Seemingly, it looks for bacteria that have already made that decision for it and uses them as a marker. Scientists had previously established that something about the bacteria P. luteoviolacea — and specifically, something made by its genes — can trigger metamorphosis of H. elegans. Then last year, scientists at Cal Tech and the University of Hawaii at Manoa reported that the aforementioned strange bristling arrays manufactured by P. luteoviolacea are necessary, though perhaps not sufficient, for a tubeworm larva to settle down.

Curious to learn more, they investigated the structure, appearance, and function of these strange structures. The arrays comprise about 100 hypodermic-needle-like structures that are in fact the baseplates, tails, and tail fibers from bacteriophage, viruses that attack and kill bacteria and are famous for their resemblance to Apollo-era lunar landers. These viruses use these tails in sinister fashion to inject their DNA into an unsuspecting host bacterium.

Tevenphage.svg
Tevenphage” by Adenosine (original); en:User:Pbroks13 (redraw) – http://commons.wikimedia.org/wiki/Image:Tevenphage.png. Licensed under CC BY-SA 2.5 via Wikimedia Commons.

Somehow, these bacteria have stolen the genes for making just the injecting tail tube, tail fibers, and base plate, but not the polyhedral head capsule. Once assembled into half a virus, they turn them upside down and join them into hemispherical arrays united at a rather amorphous base and then rejoined at the end by their tail fibers and an as-yet-unidentified protein into a hexagonal mesh or lattice. Without the genes for the sheath, tube and baseplate, P. luteoviolacea could not induce metamorphosis in H. elegans in the lab, the scientists found. The scientists dubbed these “MACs” (Metamorhposis-Associated Contractile structure) for their effects on tube worm larvae. To their knowledge, nothing like this structure has been seen before.

Here’s a movie without the computer reconstruction superimposed so you can get a better idea of what they look like under the microscope.

Oddly, the bacteria only seemed to produce the complex structures — and they seemed to stuff the cell with as many of them as they could — just prior to committing suicide and rupturing, leaving the structures free in the environment. Only about 2.4% of the cells in lab populations did this. The MAC arrays are more tightly packed inside the cell than without, hinting they they expand when the cell dies and breaks up. In addition, in tests, gently purified MAC arrays were able to induce metamorphosis in H. elegans even in the absence of living P. luteoviolacea cells.

In the diagram below, the yellow circle section is the base of the MAC array. The viral base plate looks like a maroon table, while the orange tail fibers point back in and look like they’ve joined hands.

Individual viral tail tubes in the array can move, just as they can in injecting bacteriophage viruses, and were found in several positions. The tubes themselves are actually composed of two units: an inner projectile tube (think of it as the spear) and an outer sheath (the spear launcher). Ordinarily, the sheath contracts to eject the tube, which inserts the virus’s DNA into a host. In this case, there is no DNA, at least that we’re aware of.

The tube might be present without a sheath (T), or be fully encased in a sheath (E), the sheath could have contracted but the tube not budged (J), or extended from the contracted sheath(C), or the sheath could be contracted with no tube inside at all(S). Position T may be only half-built MACs. Position “E” may be the fully armed and operational configuration, while C and S represent successful launches where the tube either remained in place after deployment or fully cleared the sheath. Js may represent jams, or misfires. The numbers next to the letters indicate how often each configuration was counted in their sample.

Fig. 4E from Shikuma et al. 2014. Click image for link.

And here’s what these possibilities looked like under the microscope. They have the same labels as in the diagram above (T, E, J, C, and S). In addition, you can clearly see the virus base plate (B) and tail fibers (TF). When the sheath is contracted, its surface texture appears helical, while when extended, it looks even. You can see this both in the diagram above and in the photos below.

Fig. 4A-D from Shikuma et al. 2014. Click image for link.

So what the heck is this thing FOR? The short answer is: we don’t know.

As I mentioned earlier, the bristly MAC arrays are made by bacteria just before death. When the cells die and rupture, the arrays are released to the environment and expand, similar to how launched satellites unfold once they reach space. We don’t know why the bacteria build them. We also don’t know exactly how H. elegans interacts with them.

The scientists had some hypotheses, though. Linking the fibers together via the hexagonal net might enable MAC arrays to coordinate their firing and deliver the biggest bang per bump; in the fired arrays the scientists looked at, all the fired fibers were clustered together physically.

There has to be some strong evolutionary pressure favoring MAC array formation by P. luteoviolacea — making them entails the ultimate price: suicide. It’s possible the bacteria make them for a purpose that is entirely unrelated to the use that the tubeworms have made of them. It’s actually not uncommon for bacteria to possess virus genes and pieces of bacteriophage they’ve made from them. They often use these to stab and kill other bacteria. So the team put P. luteoviolacea MAC extracts into containers with related bacteria to see if they could kill them. They could not. Yet there could be other kinds of MAC or other conditions under which they do.

It’s also far from clear how inducing tubeworms to settle down nearby might benefit the bacteria, if at all. MACs have been found to interact with animals before. Bacterial MACs cause loss of appetite in grass grubs and can kill wax moths. But all of the known MAC-animal interactions harm the animals in question, so the MAC blossom-tube worm relationship is something new in this respect too. P. luteoviolacea also induces coral and sea urchin larva metamorphosis.

Finally, it’s important to note that P. luteoviolacea is part of a community of microbes that make a surface”biofilm” on any freshly exposed hard surfaces in the ocean, whether that’s a ship hull or a naked rock, and, as mentioned, they produce the metamorphosis-inducing cues for a wide variety of invertebrates. So this process — disparagingly called “biofouling” on ships — is actually essential to establishing healthy coral reefs and keep the ocean running smoothly.

So it’s our own damn fault for putting shiny ship hulls into an organic soup programmed to conquer them instantly. But with knowledge of processes and structures like MAC arrays that trigger the cavalcade of encrustation, we may ultimately find a way to halt the process in a simple, elegant way, saving boatloads of dollars and needless carbon dioxide emissions. One of the funders of this fascinating research on a beautiful and obscure sub-cellular structure engaged in some sort of astounding evolutionary tango with a tiny tube worm was none other than the United States Navy.

Reference
Shikuma N.J., G. L. Weiss, M. G. Hadfield, G. J. Jensen & D. K. Newman (2014). Marine Tubeworm Metamorphosis Induced by Arrays of Bacterial Phage Tail-Like Structures, Science, 343 (6170) 529-533. DOI: http://dx.doi.org/10.1126/science.1246794