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Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

Lamanna, Francesco and Hervas-Sotomayor, Francisca and Oel, A. Phillip and Jandzik, David and Sobrido-Cameán, Daniel and Martik, Megan L. and Green, Stephen A. and Brüning, Thoomke and Mößinger, Katharina and Schmidt, Julia and Schneider, Celine and Sepp, Mari and Murat, Florent and Smith, Jeramiah J. and Bronner, Marianne E. and Rodicio, María Celina and Barreiro-Iglesias, Antón and Medeiros, Daniel M. and Arendt, Detlev and Kaessmann, Henrik (2022) Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas. bioRxiv . (Submitted) https://resolver.caltech.edu/CaltechAUTHORS:20220302-893068044

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Abstract

The vertebrate brain emerged more than ~500 million years ago in common evolutionary ancestors. To systematically trace its cellular and molecular origins, we established a spatially resolved cell type atlas of the entire brain of the sea lamprey - a jawless species whose phylogenetic position affords the reconstruction of ancestral vertebrate traits - based on extensive single-cell RNA-seq and in situ sequencing data. Comparisons of this atlas to neural data from the mouse and other jawed vertebrates unveiled various shared features that enabled the reconstruction of the core cell type composition, tissue structures, and gene expression programs of the ancestral brain. However, our analyses also revealed key tissues and cell types that arose later in evolution. For example, the ancestral vertebrate brain was likely devoid of cerebellar cell types and oligodendrocytes (myelinating cells); our data suggest that the latter emerged from astrocyte-like evolutionary precursors on the jawed vertebrate lineage. Our work illuminates the cellular and molecular architecture of the ancestral vertebrate brain and provides a foundation for exploring its diversification during evolution.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2022.02.28.482278DOIDiscussion Paper
https://www.ebi.ac.uk/arrayexpress/Related ItemRaw and processed bulk and single-cell RNA-seq data
https://lampreybrain.kaessmannlab.org/Related ItemLamprey brain atlas
https://github.com/f-lamanna/LampreyBrainAtlasRelated ItemCode
ORCID:
AuthorORCID
Lamanna, Francesco0000-0002-0447-759X
Oel, A. Phillip0000-0003-4062-0987
Jandzik, David0000-0002-4239-0014
Sobrido-Cameán, Daniel0000-0001-8239-2965
Martik, Megan L.0000-0003-1186-4085
Sepp, Mari0000-0003-1733-8385
Murat, Florent0000-0003-2116-2511
Smith, Jeramiah J.0000-0001-5333-5531
Bronner, Marianne E.0000-0003-4274-1862
Rodicio, María Celina0000-0002-7267-3285
Barreiro-Iglesias, Antón0000-0002-7507-080X
Medeiros, Daniel M.0000-0002-8182-6028
Arendt, Detlev0000-0001-7833-050X
Kaessmann, Henrik0000-0001-7563-839X
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. We thank all members of the Kaessmann group for the fruitful discussions; Elisa Panzariello, Marta Sanchez-Delgado, Nils Trost for the brain and animal illustrations, Moritz Mall for providing temporary lab-space and assistance, and Margarida Cardoso-Moreira for discussions and comments on the manuscript. Computations were performed on the Kaessmann lab server (managed by Nils Trost) and the bwForCluster from the Heidelberg University Computational Center (supported by the state of Baden-Württemberg through bwHPC and the German Research Foundation – INST 35/1134-1 FUGG). This research was supported by grants from the European Research Council (615253, OntoTransEvol), European Commission (Marie Skłodowska-Curie Actions ITN: EvoCELL), and the Tschira foundation, which funded the Illumina NextSeq machine used for sequencing. DMM and DJ were supported by the grants of National Science Foundation (IOS 1656843), National Institutes of Health/National Institute of Dental and Craniofacial Research (RDE025940), and University of Colorado, Boulder RIO Innovative Seed Grant FY21 (all to DMM). DJ was also supported by the grant from the Scientific Grant Agency of the Slovak Republic (VEGA 1/0450/21). Author contributions: F.L, F.H.-S., and H.K. conceived and organized the study based on H.K.’s original design. F.L, F.H.- S., and H.K wrote the manuscript with input from all authors. F.L. performed all analyses, and developed the brain atlas app. F.H.-S. established and optimized the tissue dissociation protocol, and performed all scRNA-seq and in situ experiments with support from A.P.O., J.S., and C.S., and guidance from M.S. F.L. and F.H.-S. annotated and interpreted the data. T.B. prepared bulk libraries with guidance from K.M. M.S. established the smFISH protocol. F.H.-S., A.P.O., D.J., D.S.C., M.L.M, and S.A.G. collected the samples. A.B.I., D.M.M., M.B., and M.C.R. provided samples. J.J.S. provided early access to genome assemblies and annotations. A.P.O., M.S., F.M., D.S.C., A.B.I., D.M.M., and D.A. provided useful feedback and discussions. H.K. supervised the study and provided funding. Data availability: Raw and processed bulk and single-cell RNA-seq data have been deposited to ArrayExpress with the accession numbers E-MTAB-11085 (bulk) and E-MTAB-11087 (single cell) (https://www.ebi.ac.uk/arrayexpress/). Additional data are available as supplementary information or upon request. Information about gene expression, cell type annotation, and gene orthology relationships across species can be visualized using the online atlas (https://lampreybrain.kaessmannlab.org/). Code availability: All code underlying the published atlas is available on GitHub (https://github.com/f-lamanna/LampreyBrainAtlas/) together with detailed instructions about its usage. Additional code is available upon request. The authors have declared no competing interest.
Funders:
Funding AgencyGrant Number
state of Baden-WürttembergUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)INST 35/1134-1 FUGG
European Research Council (ERC)615253
Marie Curie FellowshipUNSPECIFIED
Klaus Tschira FoundationUNSPECIFIED
NSFIOS-1656843
NIHRDE025940
University of Colorado, BoulderUNSPECIFIED
Slovak Research and Development AgencyVEGA 1/0450/21
DOI:10.1101/2022.02.28.482278
Record Number:CaltechAUTHORS:20220302-893068044
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220302-893068044
Official Citation:Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas Francesco Lamanna, Francisca Hervas-Sotomayor, A. Phillip Oel, David Jandzik, Daniel Sobrido-Cameán, Megan L. Martik, Stephen A. Green, Thoomke Brüning, Katharina Mößinger, Julia Schmidt, Celine Schneider, Mari Sepp, Florent Murat, Jeramiah J. Smith, Marianne E. Bronner, María Celina Rodicio, Antón Barreiro-Iglesias, Daniel Meulemans Medeiros, Detlev Arendt, Henrik Kaessmann bioRxiv 2022.02.28.482278; doi: https://doi.org/10.1101/2022.02.28.482278
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:113678
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:02 Mar 2022 10:38
Last Modified:24 Oct 2022 23:15

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  • Lamanna, Francesco and Hervas-Sotomayor, Francisca and Oel, A. Phillip and Jandzik, David and Sobrido-Cameán, Daniel and Martik, Megan L. and Green, Stephen A. and Brüning, Thoomke and Mößinger, Katharina and Schmidt, Julia and Schneider, Celine and Sepp, Mari and Murat, Florent and Smith, Jeramiah J. and Bronner, Marianne E. and Rodicio, María Celina and Barreiro-Iglesias, Antón and Medeiros, Daniel M. and Arendt, Detlev and Kaessmann, Henrik Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas. (deposited 02 Mar 2022 10:38) [Currently Displayed]

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