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Evolutionary assembly of cooperating cell types in an animal chemical defense system

Brückner, Adrian and Badroos, Jean M. and Learsch, Robert W. and Yousefelahiyeh, Mina and Kitchen, Sheila A. and Parker, Joseph (2021) Evolutionary assembly of cooperating cell types in an animal chemical defense system. bioRxiv . https://resolver.caltech.edu/CaltechAUTHORS:20211217-183447306

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Abstract

A long-standing challenge in biology is explaining how the functions of multicellular organs emerge from the underlying evolution of cell types. We deconstructed evolution of an organ novelty: a rove beetle gland that secretes a defensive cocktail. We show that gland function was pieced together via assembly of two cell types that manufacture distinct compounds. One cell type forms a chemical reservoir in the beetle’s abdomen and produces alkane and ester compounds. We demonstrate that this cell type is a hybrid of cuticle cells and ancient pheromone and adipocyte-like cells, and executes its function via a mosaic of enzymes sourced from each parental cell type. The second cell type synthesizes noxious benzoquinones using a chimeric pathway derived from conserved cellular energy and cuticle formation pathways. We present evidence that evolution of each cell type was shaped by coevolution between the two cell types: the benzoquinones produced by the second cell type dissolve in solvents produced by the first, yielding a potent secretion that confers adaptive value onto the gland as a whole. Our findings illustrate how cooperation between cell types can arise, generating new, organ-level behaviors.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.05.13.444042DOIbioRXiv Discussion Paper
https://doi.org/0.1016/j.cell.2021.11.014DOIPublished article in Cell
https://doi.org/10.22002/D1.1915DOIData: processed scRNAseq 10x data
https://doi.org/10.22002/D1.1900DOIData: processed SMARTseq data
https://doi.org/10.22002/D1.1905DOIData: raw rheology video data
https://doi.org/10.22002/D1.1914DOIData: transcriptome data
https://doi.org/10.22002/D1.1917DOIData: RNAi experiments, survival assays, in vitro
https://doi.org/10.22002/D1.1916DOIData: alignment and tree fasta files
https://doi.org/10.22002/D1.1918DOICode: Detailed code for scRNAseq analyses with Seurat and cNMF; video analyses of rheology data; custom R scripts for SMARTseq analyses via sleuth, GOterm assignments and survival data analysis
https://www.biorxiv.org/content/biorxiv/early/2021/05/15/2021.05.13.444042/DC1/embed/media-1.docx?download=truePublisherSupplemental Table S1
ORCID:
AuthorORCID
Brückner, Adrian0000-0002-9184-8562
Badroos, Jean M.0000-0002-0867-3686
Learsch, Robert W.0000-0001-6329-5879
Yousefelahiyeh, Mina0000-0003-0365-3018
Kitchen, Sheila A.0000-0003-4402-8139
Parker, Joseph0000-0001-9598-2454
Additional Information:Posted May 15, 2021. Author contributions: AB and JP designed the study. AB performed experiments with help from JP (microdissections), JMB (in vitro protein studies) and MY (microinjections). RWL performed rheological measurements and processed raw data, AB analyzed the data with input from SAK. SAK performed GO-term analysis. JP supervised the project. AB and JP wrote the manuscript with input from SAK, JMB and RWL. All authors discussed and commented on the manuscript. Acknowledgements: We thank Yuriko Kishi, Tom Naragon and Julian Wagner for help with in situ HCR, transcriptome assembly and bioinformatics, respectively; Fan Gao, Lior Pachter and the Bioinformatics Resource Center at Caltech; Sisi Chen, Jong H. Park, Matt Thomson and the Single Cell Profiling and Engineering Center (SPEC) in the Beckman Institute at Caltech; Melanie Spero for help with bacterial experiments and Chelsey M. VanDrisse for providing reagents. We are grateful to Marianne Bronner, Michael Dickinson, Lior Pachter and members of the Parker lab for feedback on this paper. AB is a Simons Fellow of the Life Sciences Research Foundation (LSRF). This work was supported by a Rita Allen Foundation Scholars Award, an Alfred P. Sloan Research Fellowship, a Shurl and Kay Curci Foundation grant, a Klingenstein-Simons Fellowship Award and a National Science Foundation CAREER award (NSF 2047472) to JP. Data availability: Raw sequence reads related to this manuscript have been deposited on NCBI under the BioProject ‘RNAseq (10x and SMARTseq) of the tergal gland of Dalotia coriaria’ (Accession: PRJNA707010; ID: 707010). All other data was uploaded to CaltechData: https://doi.org/10.22002/D1.1915 (processed scRNAseq 10x data), https://doi.org/10.22002/D1.1900 (processed SMARTseq data), https://doi.org/10.22002/D1.1905 (raw rheology video data), https://doi.org/10.22002/D1.1914 (transcriptome data), https://doi.org/10.22002/D1.1917 (RNAi experiments, survival assays, in vitro enzyme data), and https://doi.org/10.22002/D1.1916 (alignment and tree fasta files). Code availability: Detailed code for scRNAseq analyses with Seurat and cNMF; video analyses of rheology data; custom R scripts for SMARTseq analyses via sleuth, GOterm assignments and survival data analysis can be found on CaltechData (https://doi.org/10.22002/D1.1918). All other statistical comparisons using ANOVAs, Kruskal-Wallis tests, U-tests and simple ordinations were done in Past 3.04 (Hammer et al., 2001).
Funders:
Funding AgencyGrant Number
Rita Allen Foundation Scholars AwardUNSPECIFIED
Alfred P. Sloan Research FellowshipUNSPECIFIED
Shurl and Kay Curci FoundationUNSPECIFIED
Klingenstein-Simons Fellowship AwardUNSPECIFIED
NSF CAREER Award2047472
DOI:10.1101/2021.05.13.444042
Record Number:CaltechAUTHORS:20211217-183447306
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211217-183447306
Official Citation:Evolutionary assembly of cooperating cell types in an animal chemical defense system Adrian Brückner, Jean M. Badroos, Robert W. Learsch, Mina Yousefelahiyeh, Sheila A. Kitchen, Joseph Parker bioRxiv 2021.05.13.444042; doi: https://doi.org/10.1101/2021.05.13.444042
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112505
Collection:CaltechAUTHORS
Deposited By: Katherine Johnson
Deposited On:22 Nov 2022 21:38
Last Modified:22 Nov 2022 21:38

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