The world is full of unexpected relationships.
Every evening, nocturnal Hawaiian bobtail squids (Euprymna scolopes)
emerge from their burrows in shallow waters of the Pacific to hunt for
shrimp. These soft-bodied, golf-ball-size cephalopods don’t have much to
protect them from predators such seals, eels, and fish. So they rely on
another organism to help out: the bacterium Vibrio fischeri.
This microbe lives in an organ embedded in the squid’s ink sac and emits
light throughout the night to match the illumination of the moon.
Discover "What the Body Holds"
In the third chapter of “Inheritance,” the Black body is an instrument, a canvas, and a reclamation.
“It is basically acting like a little invisibility cloak for the squid,” said Jamie Foster,
a microbiologist at the Space Life Sciences Lab at the University of
Florida. In return for help with camouflage that protects against
predators, the squid offers up sugars to feed the bacteria and lure them
into the organ.
This
mutually beneficial relationship has evolved over millions of years and
is one of numerous examples of how multicellular animals and microbes
work together to increase their chances of survival. But scientists
still know little about how these relationships evolve or what spurs
animals to grow specialized organs that encourage these symbioses.
Now
Foster and an international team of researchers have mapped the genome
of a Hawaiian bobtail squid, creating a new tool to explore these
questions. By parsing the squid’s genome, the team has already
discovered that the evolution of its light organ followed a completely
different pathway than that of a second symbiotic organ, which supports
reproduction. Published in the Proceedings of the National Academy of Sciences, the findings lay the groundwork for future studies of animal-microbe interactions, including those in humans.
This
work also marks the completion of the first genome for a squid—and only
the second for a cephalopod of any kind, following the publication of a
genome map for the octopus in 2015. “Having the genome available will
be a tremendous resource for the field of studying symbiotic relations,”
said Cliff Ragsdale, a researcher at the University of Chicago who helped map the octopus genome but wasn’t involved in this new study.
Given
their tentacles, color-changing skin, and other biological novelties,
bobtail squids may not seem like the most obvious candidates for helping
with the study of symbiosis in humans or other animals. But scientists
have studied this species as a model of symbiosis for more than three
decades. “We share a lot of genes, and we share a lot of [genetic]
pathways, so we can learn a lot from these model systems about our own
health,” Foster said. For example, she noted, humans and squids share
some of the same immune-system components. In fact, our immune systems
are so comparable that Foster sends squids into space to learn more
about the human immune response to space flight.
In
addition to these helpful commonalities, the bobtail squid has a unique
quality that lends itself to symbiosis studies. Rather than going into
partnership with a consortium of bacteria, as the human gut and most
other symbiotic organs do throughout nature, the bobtail squid’s light
organ cultivates a strictly monogamous relationship with V. fischeri.
The squid’s immune system recognizes and nurtures only this one type of
bacteria within the light organ, warding off all other suitors.
“Because we just have one host and one symbiont, it is easier for us to
tease apart what is going on,” said Spencer Nyholm, a symbiosis specialist at the University of Connecticut and a co-author of the study.
With
the genome now mapped, researchers can take the next step and explore
the origins of the anatomical sites where these relationships unfold. In
the case of the light organ, the squid had to be able to monitor and
regulate the light it emits to match the light in the sky. “They needed a
way to basically do a similar thing as the eye,” Nyholm said. And,
indeed, the team found active genes in the light organ that are also
used extensively in the squid’s eye, including ones that produce a high
concentration of reflective proteins called reflectins. The squid seems
to have duplicated and modified genes it already had available to create
this helpful new organ—which also happens to include an eyelike lens.
The
second symbiotic organ the team studied, the accessory nidamental gland
(ANG), arose in a different way. The ANG is found only in females, and
it produces a gelatinous, bacteria-laden coating that protects the
squid’s eggs from being befouled by other colonizing microbes. The organ
houses many types of bacteria, and it intensely expresses novel genes
that are active nowhere else in the bobtail squid’s body—nor in any
other squid. “It had to make up these genes in order for this organ to
evolve,” Nyholm said.
While
the two organs evolved separately, they both appear to have sprung into
being relatively recently in squid evolution—roughly 30 million years
ago, in the case of the light organ. That’s roughly 240 million years
after squids and octopuses diverged.
“I think it’s a tremendous contribution,” said Angela Douglas, an entomologist who studies symbiosis at Cornell University and the author of the book The Symbiotic Habit. She
noted that, with the genome, researchers should be able to rule out
certain scenarios about how these organs evolved and dig deeper into how
animals form healthy relationships with their microbes.
“We
have this paradigm that ‘microbes are bad,’ ‘cleanliness is next to
godliness,’ and that animals are supremely good at detecting
microorganisms and killing them,” Douglas said. And yet many creatures
commonly provide a habitat for microorganisms. “Not only do we tolerate
them,” she added, “but we actually need them.”
The new genome will also help researchers study how microbes influence host evolution and vice versa, said David Bourne, a marine biologist at James Cook University in North Queensland, Australia, and the author of a recent mBio paper documenting evidence for this type of co-evolution across a variety of
marine species. “The mind-boggling diversity and abundance of microbes
makes it daunting to begin to understand these concepts of
co-evolution,” he said. But the simplicity of the bobtail-squid model,
and now the availability of the genome, will help unravel some of this
complexity.
The
different ways organisms rely on microbes go far beyond camouflage and
egg protection. For example, honeybees rely on eight different types of
gut bacteria to stay healthy, and aphids rely on bacteria to produce
amino acids they can’t readily find in their diets, according to Nancy Moran, an evolutionary biologist at the University of Texas at Austin, who edited the new paper. In Moran’s genomic studies of aphids,
she has found that the insects build their amino-acid-producing organ
with a combination of recycled genes and new ones—“or at least they have
evolved so much that you can’t see what they are related to anymore,”
she said.
In addition to
feeding and housing their microbes, animal hosts have evolved to support
the beneficial work they do. Researchers think the bobtail squid might
use its ink sac like a camera shutter to regulate the amount of light
coming out, Nyholm said. And some of the squid’s blood cells seem to
make their way into the light organ and sacrifice themselves, releasing
sugar granules in the process. The bacteria then use the sugar for
fermentation, which creates an acidic environment that helps the
bacteria’s light-producing enzyme, luciferase, generate light.
Humans
have evolved specific microenvironments that support microbial activity
too, Nyholm pointed out. The stomach is quite acidic, whereas the colon
is more alkaline—and the different microbial communities in each organ
prosper under these respective conditions. As in the squid, the human
immune system has evolved to recognize and welcome its symbionts in
these different locations.
But
when signals go awry and our immune system can’t recognize these
beneficial bacteria, conditions like inflammatory bowel disease and
other immune disorders can arise, Nyholm noted. So by understanding how
squids communicate with their bacteria in these different environments,
researchers may eventually come to understand the basis of some of these
immune diseases, he said.
The
advantage of studying this symbiosis in the squid is its natural
simplicity: While the human gut teems with diverse microbes and is hard
to view, the squid’s light organ has a one-on-one relationship with V. fischeri and is surrounded by transparent skin. “The squid system is exquisite
for being able to actually watch the bacteria enter the host,” said Mark Mandel,
a microbiologist at the University of Wisconsin at Madison, who studies
microbial symbiosis in bobtail squids as an analogue for other systems
and was not involved in this study.
To
take the next step in understanding how animals communicate with their
microbes, researchers are now working to develop methods to manipulate
and knock out genes in squid to explore which ones are essential to
which functions. “You can start asking bigger questions,” Foster said.
And
with several other cephalopod genomes in the pipeline for
completion—including those belonging to the giant squid, the blue-ringed
octopus, and others—and with the technology to produce these more
easily than in the past, researchers will soon be better equipped to
sleuth out what’s unique to the bobtail squid and what might be more
universal among cephalopods and other animals, Ragsdale said.
Once these other genomes become available, likely within the next several years, he added, “that will really open up the field.”