Squid and octopus genome studies reveal how cephalopods' unique traits
evolved

Date:
May 4, 2022
Source:
Marine Biological Laboratory
Summary:
Squid, octopus, and cuttlefish -- even to scientists who study them
- - are wonderfully weird creatures. Known as the soft-bodied or
coleoid cephalopods, they have the largest nervous system of any
invertebrate, complex behaviors such as instantaneous camouflage,
arms studded with dexterous suckers, and other evolutionarily
unique traits. Now, scientists have dug into the cephalopod genome
to understand how these unusual animals came to be. Along the way,
they discovered cephalopod genomes are as weird as the animals
are. Scientists from the Marine Biological Laboratory (MBL) in
Woods Hole, the University of Vienna, the University of Chicago,
the Okinawa Institute of Science and Technology and the University
of California, Berkeley, reported their findings in two new studies
in Nature Communications.



FULL STORY ========================================================================== Squid, octopus, and cuttlefish -- even to scientists who study them --
are wonderfully weird creatures. Known as the soft-bodied or coleoid cephalopods, they have the largest nervous system of any invertebrate,
complex behaviors such as instantaneous camouflage, arms studded with
dexterous suckers, and other evolutionarily unique traits.


==========================================================================
Now, scientists have dug into the cephalopod genome to understand
how these unusual animals came to be. Along the way, they discovered
cephalopod genomes are as weird as the animals are. Scientists from
the Marine Biological Laboratory (MBL) in Woods Hole, the University of
Vienna, the University of Chicago, the Okinawa Institute of Science and Technology and the University of California, Berkeley, reported their
findings in two new studies in Nature Communications.

"Large and elaborate brains have evolved a couple of times," said co-lead author Caroline Albertin, Hibbitt Fellow at the MBL. "One famous example
is the vertebrates. Another is the soft-bodied cephalopods, which serve as
a separate example for how a large and complicated nervous system can be
put together. By understanding the cephalopod genome, we can gain insight
into the genes that are important in setting up the nervous system, as
well as into neuronal function." In Albertin et al., published this week,
the team analyzed and compared the genomes of three cephalopod species --
two squids (Doryteuthis pealeii and Euprymna scolopes) and an octopus
(Octopus bimaculoides).

Sequencing these three cephalopod genomes, never mind comparing them,
was a tour de force effort funded by the Grass Foundation that took
place over several years in labs around the world.

"Probably the greatest advance in this new work is providing
chromosomal-level assemblies of no less than three cephalopod genomes,
all of which are available for study at the MBL," said co-author Clifton Ragsdale, professor of Neurobiology and of Biology and Anatomy at the University of Chicago.



========================================================================== "Chromosomal-level assemblies allowed us to better refine what genes are
there and what their order is, because the genome is less fragmented,"
Albertin said.

"So now we can start to study the regulatory elements that may be driving expression of these genes." In the end, comparing the genomes led the scientists to conclude that evolution of novel traits in soft-bodied cephalopods is mediated, in part, by three factors:
* massive reorganization of the cephalopod genome early in evolution
* expansion of particular gene families * large-scale editing of
messenger RNA molecules, especially in nervous
system tissues.

Most strikingly, they found the cephalopod genome "is incredibly churned
up," Albertin said.

In a related study (Schmidbaur et al.), published last week, the team
explored how the highly reorganized genome in Euprymna scolopes affects
gene expression.

The team found that the genome rearrangements resulted in new interactions
that may be involved in making many of the novel cephalopod tissues,
including their large, elaborate nervous systems.

"In many animals, gene order within the genome has been preserved over evolutionary time," Albertin said. "But in cephalopods, the genome has
gone through bursts of restructuring. This presents an interesting
situation: genes are put into new locations in the genome, with new
regulatory elements driving the genes' expression. That might create opportunities for novel traits to evolve." What's so Striking about
Cephalopod Genomes?


==========================================================================
Key insights into cephalopod genomes that the studies provide include:
They're large.The Doryteuthisgenome is 1.5 times larger than the human
genome, and the octopus genome is 90% the size of a human's.

They're scrambled."Key events in vertebrate evolution, leading to humans, include two rounds of whole-genome duplication," Ragsdale said. "With
this new work, we now know that the evolution of soft-bodied cephalopods involved similarly massive genome changes, but the changes are not
whole-genome duplications but rather immense genome rearrangements, as if
the ancestral genomes were put in a blender." "With this new information,
we can begin to ask how large-scale genome changes might underlie those
key unique features that cephalopods and vertebrates share, specifically
their capacity for large bodies with disproportionately large brains,"
Ragsdale said.

Surprisingly, they found the three cephalopod genomes are highly
rearranged relative to each other -- as well as compared to other animals.

"Octopus and squid diverged from each other around 300 million years ago,
so it makes sense that they seem they have very separate evolutionary histories," Albertin said. "This exciting result suggests that the
dramatic rearrangements in cephalopod genomes have produced new gene
orders that were important in squid and octopus evolution." They contain
novel gene families.The team identified hundreds of genes in novel
gene families that are unique to cephalopods. While some ancient gene
orders common to other animals are preserved in these new cephalopod gene families, the regulation of the genes appears to be very different. Some
of these cephalopod-specific gene families are highly expressed in unique cephalopod features, including in the squid brain.

Certain gene families are unusually expanded."An exciting example of that
is the protocadherin genes," Albertin said. "Cephalopods and vertebrates independently have duplicated their protocadherins, unlike flies and
nematodes, which lost this gene family over time. This duplication
has resulted in a rich molecular framework that perhaps is involved
in the independent evolution of large and complex nervous systems in vertebrates and cephalopods." They also found species-specific gene
family expansions, such as the genes involved in making the squid's beak
or suckers. "Neither of these gene families were found in the octopus. So, these separate groups of animals are coming up with novel gene families
to accomplish their novel biology," Albertin said.

An octopus emerges video: https://youtu.be/8F020iUEafU RNA Editing:
Another Arrow in the Quiver to Generate Novelty Prior research at the
MBL has shown that squid and octopus display an extraordinarily high rate
of RNA editing, which diversifies the kinds of proteins that the animals
can produce. To follow up on that finding, Albertin et al.sequenced RNA
from 26 different tissues in Doryteuthisand looked RNA editing rates
across the different tissues.

"We found a very strong signal for RNA editing that changes the sequence
of a protein to be restricted to the nervous system, particularly in
the brain and in the giant fiber lobe," Albertin said.

"This catalog of editing across different tissues provides a resource to
ask follow-up questions about the effects of the editing. For example, is
RNA editing occurring to help the animal adapt to changes in temperature
or other environmental factors? Along with the genome sequences, having
a catalog of RNA editing sites and rates will greatly facilitate future
work." Video: https://youtu.be/uuTMCBErVxg Why did These Cephalopods
Make the Cut? These three cephalopod species were chosen for study given
their past and future importance to scientific research. "We can learn
a lot about an animal by sequencing its genome, and the genome provides
an important toolkit for any sort of investigations going forward,"
Albertin said.

They are:
* The Atlantic longfin inshore squid (Doryteuthis pealeii). Nearly a
century of research on this squid at the MBL and elsewhere
has revealed fundamental principles of neurotransmission (some
discoveries garnering a Nobel Prize). Yet this is the first report
of the genome sequence of this well-studied squid (in Albertin et
al.,funded by the Grass Foundation).

Two years ago, an MBL team achieved the first gene knockout
in a cephalopod using Doryteuthis pealeii, taking advantage of
preliminary genomic sequence data and CRISPr-Cas9 genome editing.

* The Hawaiian bobtail squid (Euprymna scolopes). A glowing bacterium
lives
inside a unique "light organ" in the squid, to the mutual benefit of
both. This species has become a model system for studying animal-
bacterial symbiosis and other aspects of development. A draft
E. scolopes genome assembly was published in 2019.

* The California two-spot octopus (Octopus bimaculoides). A relative
newcomer on the block of scientific research, this was the first
octopus genome ever sequenced. Albertin co-led the team that
published its draft genome in 2015.


========================================================================== Story Source: Materials provided by Marine_Biological_Laboratory. Original written by Diana Kenney. Note: Content may be edited for style and length.


========================================================================== Related Multimedia:
* Images_of_octopuses_and_squid ========================================================================== Journal References:
1. Caroline B. Albertin, Sofia Medina-Ruiz, Therese Mitros, Hannah
Schmidbaur, Gustavo Sanchez, Z. Yan Wang, Jane Grimwood, Joshua
J. C.

Rosenthal, Clifton W. Ragsdale, Oleg Simakov, Daniel
S. Rokhsar. Genome and transcriptome mechanisms driving
cephalopod evolution. Nature Communications, 2022; 13 (1) DOI:
10.1038/s41467-022-29748-w
2. Hannah Schmidbaur, Akane Kawaguchi, Tereza Clarence, Xiao Fu, Oi Pui
Hoang, Bob Zimmermann, Elena A. Ritschard, Anton Weissenbacher,
Jamie S.

Foster, Spencer V. Nyholm, Paul A. Bates, Caroline B. Albertin, Elly
Tanaka, Oleg Simakov. Emergence of novel cephalopod gene regulation
and expression through large-scale genome reorganization. Nature
Communications, 2022; 13 (1) DOI: 10.1038/s41467-022-29694-7 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2022/05/220504082333.htm

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