Menu

Close

The ancestral animal genetic toolkit revealed by diverse choanoflagellate transcriptomes

Daniel Richter, Parinaz Fozouni, Michael Eisen, Nicole King

Preprint posted on December 26, 2017 https://www.biorxiv.org/content/early/2017/12/26/211789

Which set of genes distinguishes animals from other organisms? Work from the King lab suggests we need to rewrite textbooks.

Selected by Rafael Galupa

Background

As humans, we are morphologically very different from butterflies or jellyfish, yet we belong together in the phylogenetic branch of Animalia/Metazoa, separate from other multicellular eukaryotes such as plants or fungi. So what makes up an animal? Comparing animal genomes to those of other organisms, especially their closest living relatives, choanoflagellates, can tell us which genes have specifically appeared or disappeared during animal evolution. However, only two genomes of choanoflagellate species have been sequenced to date, limiting the power of such comparisons to identify genes that are truly animal innovations.

Key findings

The authors sequenced the transcriptome of 19 choanoflagellate species, substantially increasing the available genomic information on these organisms and allowing a more refined comparison to animal genomes. This revealed:

(1) More than a thousand animal-specific gene families (including well-known developmental players such as TGF-β, Hedgehog, Pax and Sox), most of which were lost in one or more extant lineages. Only 36 gene families were found conserved across all animal genomes available, including components of the Wnt pathway and cell-cell adhesion molecules

(2) More than a thousand gene families present in the common ancestor but specifically lost in animals, reflecting changes in ecology and metabolism (e.g. pathways necessary for the biosynthesis of essential amino acids)

(3) Many gene families believed to be animal-specific are actually present in choanoflagellates, indicating that they evolved before the emergence of the animal lineages. These include Notch receptors and ligands, critical innate immunity receptors (TLRs) and enzymes involved in extracellular matrix remodelling.

What I like about this preprint

Not only the fact that the authors are asking a BIG fundamental biological question – where we came from, as animals, and what happened along the way, from a genomic perspective – but also that their study ends up challenging the current view of which genes constitute an “animal signature”, probably leading to changes in our textbooks. And who would have guessed how much we could learn from studying… choanoflagellates?! A reminder of how important it is to explore even the more unlikely organisms.

Open questions

It will be exciting to explore whether gene families common between animals and choanoflagellates serve similar biological functions in the two lineages, or whether they might have been exploited differently. For example, what could be the significance of the Notch pathway in single-cell choanoflagellates?

Curiosity corner

The authors had to optimise specific growth conditions and RNA extraction protocols for each of the 19 species of choanoflagellates they sequenced!

Tags: animal evolution, choanoflagellates, comparative genomics, metazoa

Posted on: 16th February 2018 , updated on: 9th September 2018

Read preprint (2 votes)




  • Author's response

    Daniel Richter shared

    You pose an excellent question: can we test whether gene families that evolved on the stem lineage leading to animals and choanoflagellates have similar functions in the two groups? The timing of this question is perfect, because a robust method for transfection in choanoflagellates was just developed! It was described in a preprint on bioRxiv (https://doi.org/10.1101/343111) and was even highlighted in a preLight (https://prelights.biologists.com/highlights/robust-method-transfection-choanoflagellates-illuminates-cell-biology-ancestry-animal-septins/). Using the techniques described in this preprint, it should be possible to interrogate the choanoflagellate functions of intriguing gene families that we identified, such as Notch or TLRs.
    It’s great that you pointed out the challenges in optimizing lab protocols separately for each of the 19 species we sequenced. When choanoflagellates are isolated from the environment, they are co-isolated with their bacterial prey, which may come from many different species. Each culture thus represents a mini-ecosystem that responds differently to lab manipulation, based on the biology of the choanoflagellate species and on the interactions with and among the diversity of bacterial prey species present. These optimizations were actually one of the most time-consuming parts of the project!

    Have your say

    Your email address will not be published. Required fields are marked *

    Sign up to customise the site to your preferences and to receive alerts

    Register here

    Also in the evolutionary biology category:

    PUMILIO hyperactivity drives premature aging of Norad-deficient mice

    Florian Kopp, Mehmet Yalvac, Beibei Chen, et al.



    Selected by Carmen Adriaens

    Eukaryotic acquisition of a bacterial operon

    Jacek Kominek, Drew T. Doering, Dana A. Opulente, et al.



    Selected by Lauren Neves

    millepattes micropeptides are an ancient developmental switch required for embryonic patterning

    Suparna Ray, Miriam I Rosenberg, Hélène Chanut-Delalande, et al.



    Selected by Erik Clark

    Conserved phosphorylation hotspots in eukaryotic protein domain families

    Marta J Strumillo, Michaela Oplova, Cristina Vieitez, et al.



    Selected by Gautam Dey

    Peculiar features of the plastids of the colourless alga Euglena longa and photosynthetic euglenophytes unveiled by transcriptome analyses

    Kristina Zahonova, Zoltan Fussy, Erik Bircak, et al.



    Selected by Ellis O'Neill

    1

    The Ly6/uPAR protein Bouncer is necessary and sufficient for species-specific fertilization

    Sarah Herberg, Krista R Gert, Alexander Schleiffer, et al.



    Selected by James Gagnon

    Timed collinear activation of Hox genes during gastrulation controls the avian forelimb position

    Chloe Moreau, Paolo Caldarelli, Didier Rocancourt, et al.



    Selected by Wouter Masselink

    The genomic basis of colour pattern polymorphism in the harlequin ladybird

    Mathieu Gautier, Junichi Yamaguchi, Julien Foucaud, et al.



    Selected by Fillip Port

    Altering the temporal regulation of one transcription factor drives sensory trade-offs

    Ariane Ramaekers, Simon Weinberger, Annelies Claeys, et al.



    Selected by Mariana R.P. Alves

    A robust method for transfection in choanoflagellates illuminates their cell biology and the ancestry of animal septins

    David Booth, Heather Middleton, Nicole King



    Selected by Maya Emmons-Bell

    A SoxB gene acts as an anterior gap gene and regulates posterior segment addition in the spider Parasteatoda tepidariorum

    Christian L. B. Paese, Anna Schoenauer, Daniel J. Leite, et al.



    Selected by Erik Clark

    1

    Germ layer specific regulation of cell polarity and adhesion gives insight into the evolution of mesoderm.

    Miguel Salinas-Saavedra, Amber Q. Rock, Mark Q. Martindale



    Selected by ClaireS & SophieM

    1

    Wnt/β-catenin regulates an ancient signaling network during zebrafish scale development

    Andrew J Aman, Alexis N Fulbright, David M Parichy



    Selected by Andreas van Impel

    Bacteriophage cooperation suppresses CRISPR-Cas3 and Cas9 immunity

    Adair L Borges, Jenny Y Zhang, MaryClare Rollins, et al.

    AND

    Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity

    Mariann Landsberger, Sylvain Gandon, Sean Meaden, et al.



    Selected by Fillip Port

    Dynamic Kinetochore Size Regulation Promotes Microtubule Capture And Chromosome Biorientation In Mitosis

    Carlos Sacristan, Misbha Ahmad, Jenny Keller, et al.

    AND

    Self-assembly of the RZZ complex into filaments drives kinetochore expansion in the absence of microtubule attachment

    Cláudia Pereira, Rita M Reis, José B Gama, et al.



    Selected by Gautam Dey

    Individual- and population-level drivers of consistent foraging success across environments

    Lysanne Snijders, Ralf HJM Kurvers, Stefan Krause, et al.



    Selected by Rasmus Ern

    Also in the genomics category:

    Comparative analysis of droplet-based ultra-high-throughput single-cell RNA-seq systems

    Xiannian Zhang, Tianqi Li, Feng Liu, et al.



    Selected by Samantha Seah

    PUMILIO hyperactivity drives premature aging of Norad-deficient mice

    Florian Kopp, Mehmet Yalvac, Beibei Chen, et al.



    Selected by Carmen Adriaens

    LCM-seq reveals unique transcriptional adaption mechanisms of resistant neurons in spinal muscular atrophy

    Susanne Nichterwitz, Helena Storvall, Jik Nijssen, et al.

    AND

    Axon-seq decodes the motor axon transcriptome and its modulation in response to ALS

    Jik Nijssen, Julio Cesar Aguila Benitez, Rein Hoogstraaten, et al.



    Selected by Yen-Chung Chen

    LADL: Light-activated dynamic looping for endogenous gene expression control

    Mayuri Rege, Ji Hun Kim, Jacqueline Valeri, et al.



    Selected by Ivan Candido-Ferreira

    Precise tuning of gene expression output levels in mammalian cells

    Yale S. Michaels, Mike B Barnkob, Hector Barbosa, et al.



    Selected by Tim Fessenden

    1

    Template switching causes artificial junction formation and false identification of circular RNAs

    Chong Tang, Tian Yu, Yeming Xie, et al.



    Selected by Fabio Liberante

    The genomic basis of colour pattern polymorphism in the harlequin ladybird

    Mathieu Gautier, Junichi Yamaguchi, Julien Foucaud, et al.



    Selected by Fillip Port

    Widespread inter-individual gene expression variability in Arabidopsis thaliana

    Sandra Cortijo, Zeynep Aydin, Sebastian Ahnert, et al.



    Selected by Martin Balcerowicz

    Single-cell Map of Diverse Immune Phenotypes Driven by the Tumor Microenvironment

    Elham Azizi, Ambrose J. Carr, George Plitas, et al.



    Selected by Tim Fessenden

    Cell type-specific interchromosomal interactions as a mechanism for transcriptional diversity

    Adan Horta, Kevin Monahan, Lisa Bashkirova, et al.



    Selected by Boyan Bonev

    PDX Finder: A Portal for Patient-Derived tumor Xenograft Model Discovery

    Nathalie Conte, Jeremy Mason, Csaba Halmagyi, et al.



    Selected by Carmen Adriaens

    An atlas of silencer elements for the human and mouse genomes

    Naresh Doni Jayavelu, Ajay Jajodia, Arpit Mishra, et al.



    Selected by Rafael Galupa

    1

    Capturing the onset of PRC2-mediated repressive domain formation

    Ozgur Oksuz, Varun Narendra, Chul-Hwan Lee, et al.



    Selected by Boyan Bonev

    Heterochromatin drives organization of conventional and inverted nuclei

    Martin Falk, Yana Feodorova, Natasha Naumova, et al.



    Selected by Boyan Bonev

    The ancestral animal genetic toolkit revealed by diverse choanoflagellate transcriptomes

    Daniel Richter, Parinaz Fozouni, Michael Eisen, et al.



    Selected by Rafael Galupa

    1

    Genome-wide selection scans integrated with association mapping reveal mechanisms of physiological adaptation across a salinity gradient in killifish

    Reid S. Brennan, Timothy M. Healy, Heather J. Bryant, et al.



    Selected by Andy Turko
    Close