Des créatures merveilleusement étranges : Les génomes du calmar et de la pieuvre révèlent comment les caractéristiques uniques des céphalopodes ont évolué.

Calmar côtier à long nez de l'Atlantique (Doryteuthis pealeii)

Le calmar côtier à nageoires longues de l’Atlantique, Doryteuthis pealeiiest étudié depuis près d’un siècle par les scientifiques comme un système modèle pour les recherches en neurosciences. Crédit : Elaine Bearer

Le calmar, la pieuvre et la seiche sont des créatures merveilleusement étranges, même pour les scientifiques qui les étudient. Connus sous le nom de céphalopodes à corps mou ou coléoïdes, ils possèdent le plus grand système nerveux de tous les invertébrés, des comportements complexes tels que le camouflage instantané, des bras munis de ventouses adroites et d’autres caractéristiques uniques dans l’évolution.

Aujourd’hui, les scientifiques ont creusé dans le génome des céphalopodes pour comprendre comment ces animaux inhabituels sont apparus. En cours de route, ils ont découvert que les génomes des céphalopodes sont aussi étranges que les animaux. Des scientifiques du Marine Biological Laboratory (MBL) de Woods Hole, de l’université de Vienne, de l’University of Chicago, the Okinawa Institute of Science and Technology and the University of California, Berkeley, reported their findings in two new studies published in the journal 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.”


Pieuvres californiennes à deux points (Octopus bimaculoides) émergeant de leurs enveloppes d’œufs. Crédit : Caroline Albertin, Laboratoire de biologie marine.

Dans Albertin et al., publiée cette semaine, l’équipe a analysé et comparé les génomes de trois espèces de céphalopodes – deux calmars (Doryteuthis pealeii et Euprymna scolopes) et une pieuvre (Pieuvre bimaculoides).

Le séquençage de ces trois génomes de céphalopodes, sans parler de leur comparaison, a constitué un véritable tour de force financé par la Fondation Grass et s’est déroulé sur plusieurs années dans des laboratoires du monde entier.

“La plus grande avancée de ce nouveau travail est probablement de fournir des assemblages au niveau chromosomique de pas moins de trois génomes de céphalopodes, qui sont tous disponibles pour être étudiés au MBL”, a déclaré le co-auteur Clifton Ragsdale, professeur de neurobiologie et de biologie et anatomie à l’Université de Chicago.

“Les assemblages au niveau chromosomique nous ont permis de mieux préciser quels gènes sont présents et quel est leur ordre, car le génome est moins fragmenté”, a déclaré Albertin. “Nous pouvons donc maintenant commencer à étudier les éléments de régulation qui peuvent conduire l’expression de ces gènes”.

En fin de compte, la comparaison des génomes a conduit les scientifiques à conclure que l’évolution des caractères nouveaux chez les céphalopodes à corps mou est médiée, en partie, par trois facteurs :

  • Une réorganisation massive du génome des céphalopodes au début de l’évolution.
  • l’expansion de familles de gènes particulières
  • édition à grande échelle des messagers 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 Doryteuthis genome 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.

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 Doryteuthis and 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.”

Sidebar: 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.

References:

“Genome and Transcriptome Mechanisms Driving Cephalopod Evolution” by Caroline B. Albertin, Sofia Medina-Ruiz, Therese Mitros, Hannah Schmidbaur et al 4 May 2022, Nature Communications.
DOI: 10.1038/s41467-022-29748-w

Co-authors are from the Marine Biological Laboratory (Caroline Albertin and Joshua Rosenthal), University of California-Berkeley, University of Vienna, Hiroshima University, University of Chicago, Hudson Alpha Institute of Biotechnology, Okinawa Institute for Science and Technology, and Chan-Zuckerberg Biohub.

“Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization” by 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 and Oleg Simakov, 21 April 2022, Nature Communications.
DOI: 10.1038/s41467-022-29694-7

Co-authors are from University of Vienna; Institute of Molecular Pathology, Vienna; The Frances Crick Institute; The Vienna Zoo; University of Florida; Marine Biological Laboratory; and University of Connecticut.

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