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This Squid’s Glowing Microbes Can Reprogram Its Eyes From Afar

A squid’s eye view of its own microbes shows the intimate link between a nocturnal sea-dweller and its cache of bioluminescent bacteria.

ByKatherine J. WuNOVA WondersNOVA Wonders
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Bobtail squid are never alone. Inside their bodies reside a teeming community of Vibrio fischeri bacteria. In exchange for food and housing, the bacteria emit a glow to mask the squid's silhouettes from the eyes of predators at night... and spark a cascade of changes throughout the squid's entire body. Image Credit: David_Slater, iStock

The Hawaiian bobtail squid might be small, but this walnut-sized critter is one of the sea’s mightiest masters of disguise. During its evening jaunts, the squid protects itself by casting an eerie glow to match the moonlight, obscuring its silhouette to predators lurking in the water column below.

This cloak of invisibility is an illusion by collusion, all thanks to a luminous cache of Vibrio fischeri bacteria held within a specialized chamber within the squid’s body called the light organ. In exchange for canceling out the squid’s shadow, the microbes receive housing and a stipend of sugars.

But it’s now clear that these microbes do far more than conjure a cloak of invisibility. From the moment it enters the light organ, V. fischeri sparks a cascade of changes that can even transform parts of the squid’s body, like its eyes and gills, which never physically encounter the bacteria themselves. The finding, published today in the journal PNAS, illustrates the far-reaching consequences of microbial colonization—and could illuminate similarly intimate partnerships in humans.

“This will help create a real paradigm shift,” says Bethany Rader, a microbiologist at Southern Illinois University who was not involved in the study. “It’s folly to think about health without considering how microbes influence the entire body.”

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Decades of research have shown time and time again that the microbes that inhabit animal bodies dictate countless aspects of health. Perhaps most famously, the bacteria that inhabit the mammalian large intestine—the gut microbiota—can affect everything from the way the immune system functions, to the regularity of sleep-wake cycles, to how the brain interprets information.

But what’s been far less obvious is exactly how bacteria are sending out system-wide marching orders from isolated control centers like the colon. Complicating things is the fact that thousands of microbial species inhabit the bodies of mammals like humans, making it tough to disentangle who’s responsible for what effect.

That’s where the bobtail squid comes in. Their light organs are notoriously picky: Only V. fischeri are permitted to enter, while interlopers are unceremoniously dumped back into the salty sea. “The beauty of this system is that it’s simple,” says study author Silvia Moriano-Gutierrez, a marine biologist at the University of Hawaiʻi at Mānoa. “There are only two partners at play.”

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The Hawaiian bobtail squid is the size of a walnut, but it's able to squeeze an entire population of microbes into a small sac in its body. Image Credit: Margaret McFall-Ngai and Edward Ruby, Squid Vibrio Labs, University of Hawaiʻi at Mānoa

To parse out the extent of the squid-microbe relationship, a team led by Moriano-Gutierrez reared squid with or without V. fischeri (bacteria-free individuals have never been found in the wild, but get along swimmingly in the lab). When the researchers compared gene expression in the two groups over time, they found that the presence of microbes substantially retooled cells in not just the light organ where they were housed, but also organs elsewhere in the body, such as the eyes and gills, where V. fischeri never treads. Additionally, distinct genetic patterns arose in each location, signaling that each organ had interpreted V. fischeri in its own way.

This was a striking find—akin to a guest entering an inn and simultaneously rearranging furniture behind the concierge desk, in its room upstairs, and in the dining room out back, all without leaving the foyer. As the humble patron of the Hotel Calamari, V. fischeri had shaped its surroundings on a squid-wide scale.

From the squid’s perspective, however, these might be important adjustments, says study author Margaret McFall-Ngai, a squid biologist who supervises Moriano-Gutierrez’s work. Like the light organ, the eyes and gills have stakes (albeit, indirect ones) in microbial fraternizing. A keen sense of sight helps the squid gauge how bright its surroundings are, so it can fine-tune the output from its light organ. The gills, on the other hand, play a role in squid immunity, and need to remain on high alert for bacteria in the vicinity.

And these different priorities shaped the nature of each organ’s response to the bacteria. When the researchers repeated their experiment, this time swapping out naturally glowing V. fischeri with mutants who couldn’t produce light, the bacteria elicited much less turnover in the light organ and eyes (the gills, however, didn’t seem to care either way). In other words, without their luminescence, the bacteria couldn’t trigger the normal suite of changes in the organs where light mattered most—causing the squid to turn a blind eye to their presence.

“This underscores the importance of luminousness to the animal,” McFall-Ngai says. “From their perspective, it’s the most important thing the bacteria do.”

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A dissected bobtail squid, tentacle-up. The ink sac (black) is shown in the middle; the light organ is nestled against it, looking like two kidneys stuck together. The animal's eyes are just below its tentacles, while the gills are the fluffy, whitish areas near the top of its body (bottom of the photo). All of these organs are affected by the presence of Vibrio fischeri. Image Credit: Margaret McFall-Ngai and Edward Ruby, Squid Vibrio Labs, University of Hawaiʻi at Mānoa

How exactly V. fischeri communicates with the eyes and gills is still unclear. One obvious signal for the eyes might be light itself—but the squid actually doesn’t have the best view of its own glow. And that wouldn’t explain how the gills are tuning in.

One possibility is that microbes are churning out chemical cues that enter the squid’s bloodstream, says study author Edward Ruby, a microbiologist who runs the partner lab to McFall-Ngai’s at the University of Hawaiʻi at Mānoa. Then, depending on the organ at which they arrive, the messages might be interpreted differently by the specialized cells at each site. That would be the equivalent of every service team in a hotel hearing a guest’s footsteps in the doorway: Depending on its specialty, each would be spurred onto a different course of action.

Rader, the Southern Illinois University microbiologist, proposes an alternative. Rather than sending out an all-purpose SOS, the bacteria could also be dispatching distinct instructions to individual organs—like the same hotel guest calling the kitchen’s direct line, rather than using a building-wide intercom. That way, specific memos about light, for instance, wouldn’t get wasted on the gills.

These possibilities aren’t mutually exclusive. Either way, Ruby says, it’s a reminder that there’s complexity on both sides of the equation: a multitude of bacteria producing signals, and a troupe of target tissues waiting to receive them.

These relationships are likely echoed in other animals as well—including humans, Rader says. “Squid may not look a lot like us, but we possess a lot of the same types of tissues and share [part of] our immune system,” she says. “The answers we get from squid are just as valid and informative as those from mice.”

Studies like these show us that animals more than just isolated, single bodies, says Maria Castillo, a bobtail squid researcher at New Mexico State University who was not involved in the study. Whether we like it or not, we are all growing and changing under the influence of our microbial allies, she says.

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A Hawaiian bobtail squid, scooped into a human hand. These critters can be just an inch or so long in adulthood. Image Credit: Margaret McFall-Ngai and Edward Ruby, Squid Vibrio Labs, University of Hawaiʻi at Mānoa

But all this does raise the question: In this lifelong dialogue, who’s really in charge—the squid or its Vibrio?

For McFall-Ngai and Ruby, this has historically been a point of contention. The two are professional (and romantic) partners: McFall-Ngai, a zoologist by training, represents the squid half of the equation, while Ruby bats for Team Vibrio. After decades of work, the two settled on an answer: “I’ve had to concede that the host is clearly in charge,” Ruby says.

The squid does have a lot of say in this unconventional union. Every morning, they’ll jettison about 90 percent of their resident V. fischeri before settling down to sleepessentially shutting off an unneeded nightlight. And if any bacteria fail to light up, the squid can evict the would-be freeloaders without a second thought. “If you’re not doing your job, you’re gone!” McFall-Ngai says. Microbes might be honored guests, but their hosts still have final say on checkout time.

Others, however, are a bit more hesitant to yield microbial ground. “I can’t answer that question!” Castillo says with a laugh. “They need each other.”

Rader points to the fateful first meeting of squid and bacteria. It’s unclear who makes the first move—but from day one, the two enter a conversation, rather than a dictation. Host and microbe guide each other’s development through a delicate back and forth, down to levels of chemicals, molecules, and genes.

“Really, it’s probably an equal partnership,” Rader adds. If she’s going by her gut, she says, “it’s a relationship as equal as one can be.”

But then again, maybe that’s the microbes talking.

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