Animals that take advice from bacteria



What a shame for the poor tube worm, whose life is fraught with risks. Like many marine invertebrates, the worm spends its earliest days as a tiny larva that floated in plankton – but sooner or later it will have to find a place to perch. Once cemented onto a hard surface, it begins the massive change in shape called metamorphosis from which it emerges in its magnificent adult form.

There’s no second chance: a worm that picks a bad spot can’t try again. Faced with such a momentous decision – the most important of its life – the larva needs all the help it can get. Often this help comes from a completely different realm of life.

Scientists have known for several decades that some animal larvae, including those of tube worms, select sites for metamorphosis by monitoring chemical signals released by bacteria. But they are only just beginning to realize how widespread the relationship can be and how sophisticated – sometimes using special bacterial machines to send signals to the larvae. This implies that communication between animals and bacteria in the oceans could be much richer and more cooperative than previously thought.

And there could be practical applications: experts might one day find ways to manage this communication, getting animals to settle in some places like oyster farms and discouraging them in others like the hulls of ships.

It is hardly surprising that tube worms and other planktonic larvae rely on bacterial clues to select a suitable site for metamorphosis. After all, a thin layer of mixed types of bacteria – called a biofilm – covers every available ocean surface. What is new is the emerging breadth of this phenomenon. “In every major branch of the animal tree of life, there are species that metamorphose in response to bacteria,” says Nicholas Shikuma, a microbiologist at San Diego State University, who looks at. co-authored how bacteria affect animal metamorphosis in 2021 Annual microbiology review.

Bacterial induction of metamorphosis is widespread in the animal kingdom and occurs in almost every large group of animals.

In some cases, the larvae appear to be merely listening to chemical signals released when bacteria compete with one another or otherwise go about their own business. In others, however, researchers suggest that the larvae are the primary, “intended” target for the signal. In one notable case, Shikuma’s team found a biofilm bacterium called Pseudoalteromonas luteoviolacea produces molecular syringes that actively inject a metamorphosis-inducing protein into larvae of the tube worm Hydroides elegans.

Many bacteria have syringe-like injection machines, but this is the first time they have played a role in animal metamorphosis. More often it is used to carry a lot of toxins. Some bacteria, like the ones that cause cholera, use the toxins to destroy their host’s cells. Others use them for inter-microbial warfare.

The syringes are evolutionarily related to the proteins in the tails of viruses, called bacteriophages, which invade bacteria. The viruses use the machinery to inject their genetic material into host bacteria – and at some point in the distant past bacteria must have acquired the genes and used them for their own use.

Most bacteria release their syringes one at a time, as do phages. but Pseudoalteromonas is strikingly different. Instead of a single syringe, it is creates a structure with several hundred. The bacterial cell builds up the structure in a compact, folded configuration like a piece of furniture that is taken along. Then the cell bursts and the neat package unfolds, blossoms into a hemispherical mass – the “death star”, as Shikuma likes to call it. (Only about 2.4 percent of the Pseudoalteromonas Cells in a biofilm produce the Death Star, presumably for the collective benefit of the colony.)

(Photo credit: Brian Nedved / University of Hawaii)

Each syringe tube in this Death Star contains a protein called Mif1, which induces metamorphosis in Hydroids Larvae. Most likely, the protein binds to a target within the larval cell, since extracellular Mif1 has no effect. Shikuma’s lab is trying to see if Mif1 performs other functions, such as attacking other bacteria, but they haven’t found any yet, he says – and that flaw, plus the sophisticated nature of the delivery system, makes him think that Hydroids could be the intended target of the Death Star.

When the bacteria go out of their way to help Hydroids Dropping off, that would indicate it’s getting something back, Shikuma says. He has not yet established exactly what that benefit is, but he is speculating on it by luring Hydroids settle down, Pseudoalteromonas helps ensure that its biofilm will be the first to colonize the new surfaces – the new habitat – that the tubular worm’s growing body will provide.

If he is right, or if the bacteria get some other benefit from the worms, this could change ideas about the balance of forces in the larval settlement. “People thought that the animal was in charge and that the bacteria were only serving as passive cues from the environment,” says Shikuma. “But the bacteria could benefit more from the interaction than we are currently aware of.”

A model of the “death star” produced by the bacterium Pseudoalteromonas luteoviolacea. The structure is a hemispherical arrangement with dozens of molecular syringes that inject a protein into larvae of the tube worm Hydroides elegans, triggering metamorphosis. Many bacteria use single molecular syringes, often for defense, but this much more complex system is the only one known to affect animal metamorphosis. (Image: NJ Shikuma ET AL / Science 2014)

Some other researchers are unwilling to buy the idea. “Personally, I don’t think all the evidence is there to really say there is active involvement,” says Brian Nedved, a larval biologist at the University of Hawaii who also teaches the Hydroids. Instead, Nedved thinks it is more likely that the Death Star will play an as-yet-undiscovered role in defense Pseudoalteromonas from competing bacteria. Mif1 isn’t the only factor involved, either. Other molecules can also trigger Hydroids Metamorphosis through various mechanisms, says Nedved.

Shikuma has meanwhile found the same genes involved in building the Death Star in completely unrelated types of bacteria – those that are part of the normal microbial flora in the human gut. “It is very strange that they are there and we are excited to see what they are good for,” he says.

The US Navy is interested enough to fund its work, largely because it knows why larvae of living things like Hydroids settling where they settle could lead to better ways of keeping them off the ship’s hulls. But the Navy is also intrigued by other, more futuristic options, says Shikuma, such as figuring out how to load a Death Star with therapeutic drugs – antimicrobial drugs, for example, that soldiers might one day take to prevent diarrhea in travelers.

And there’s a bigger idea at play too, says Suhelen Egan, an environmental microbiologist at the University of New South Wales, Australia who studies the interactions between seaweed and bacteria. If Shikuma is right – that marine larvae not only eavesdrop on bacteria, but actively participate in a conversation – the same could apply to many other ecosystems. And that could mean that microbial communities are much more integrated with the higher organisms on which they live than ecologists have previously recognized.

These interactions don’t have to be intimate one-on-one conversations, notes Egan. Instead, they could look more like a cocktail party, with a multitude of participants interacting with a wide variety of partners in loose, changing associations. Nobody knows yet, but the bizarre relationship between a shell-polluting tube worm and Death Star bacteria provides a good starting point to start learning.

10.1146 / knowable-092121-1

Bob Holmes is a science writer based in Edmonton, Canada.

This article originally appeared in Well-known magazine, an independent journalistic endeavor of Annual Reviews.



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