A lamprey neural cell type atlas illuminates the origins of the vertebrate brain

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Acknowledgement

We thank all members of the Kaessmann group for fruitful discussions; Robert Frömel for his help with library sequencing; E. Panzariello, M. Sanchez-Delgado and N. Trost for the brain and animal illustrations; M. Mall for providing temporary lab space; and M. Cardoso-Moreira for discussions and comments on the manuscript. The computations were performed on the Kaessmann lab server (managed by N. 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). We thank W. Wang of the Northwestern Polytechnical University of Xi'an, China; Y. Zhang of the Institute of Zoology, Chinese Academy of Sciences; and J. Pascual-Anaya from the University of Málaga, Spain, for granting access to the early draft of the inshore hagfish genome (https://doi.org/10.1101/2023.04.08.536076). This work was supported by grants from the European Research Council (no. 615253, OntoTransEvol), the European Commission (Marie Skłodowska-Curie Actions ITN: EvoCELL) and the Tschira foundation, which funded the Illumina NextSeq machine used for sequencing. D.M.M. and D.J. were supported by grants from the National Science Foundation (IOS 1656843), the National Institutes of Health/National Institute of Dental and Craniofacial Research (RDE025940) and University of Colorado, Boulder RIO Innovative Seed Grant FY21 (all to D.M.M.). D.J. was also supported by a grant from the Scientific Grant Agency of the Slovak Republic (VEGA 1/0450/21). This project has received funding from the European Research Council under the European Union's Horizon 2020 research and innovation programme (VerteBrain to H.K., grant agreement no. 101019268; and NeuralCellTypeEvo to D.A., grant agreement no. 788921).

Contributions

These authors contributed equally: Francesco Lamanna, Francisca Hervas-Sotomayor.

F.L., F.H.-S. and H.K. conceived and organized the study on the basis of 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. Schmidt and C.S. and guidance from M.S. F.L. and F.H.-S. annotated and interpreted the data. T.B. prepared the bulk libraries with guidance from K.M. M.S. established the smRNA-FISH protocol. F.H.-S., A.P.O., D.J., D.S.-C., G.N.S.-D., M.L.M., J. Stundl and S.A.G. collected the samples. A.B.-I., D.M.M., M.E.B. and M.C.R. provided the 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

The raw and processed bulk and scRNA-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/). The genome annotation files and in situ images have been deposited to Zenodo110 (https://doi.org/10.5281/zenodo.5903844). 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/) and Zenodo111 (https://doi.org/10.5281/zenodo.8113793) together with detailed instructions about its usage.

Conflict of Interest

The authors declare no competing interests.