Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins
The identity and function of a given cell type relies on the differential expression of gene batteries that promote diverse phenotypes and functional specificities. Therefore, the identification of the molecular and morphological fingerprints of cell types across taxa is essential for untangling the...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2022.991664/full |
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| author | Periklis Paganos Paolo Ronchi Jil Carl Giulia Mizzon Pedro Martinez Pedro Martinez Giovanna Benvenuto Maria Ina Arnone |
| author_facet | Periklis Paganos Paolo Ronchi Jil Carl Giulia Mizzon Pedro Martinez Pedro Martinez Giovanna Benvenuto Maria Ina Arnone |
| author_sort | Periklis Paganos |
| collection | DOAJ |
| description | The identity and function of a given cell type relies on the differential expression of gene batteries that promote diverse phenotypes and functional specificities. Therefore, the identification of the molecular and morphological fingerprints of cell types across taxa is essential for untangling their evolution. Here we use a multidisciplinary approach to identify the molecular and morphological features of an exocrine, pancreas-like cell type harbored within the sea urchin larval gut. Using single cell transcriptomics, we identify various cell populations with a pancreatic-like molecular fingerprint that are enriched within the S. purpuratus larva digestive tract. Among these, in the region where they reside, the midgut/stomach domain, we find that populations of exocrine pancreas-like cells have a unique regulatory wiring distinct from the rest the of the cell types of the same region. Furthermore, Serial Block-face scanning Electron Microscopy (SBEM) of the exocrine cells shows that this reported molecular diversity is associated to distinct morphological features that reflect the physiological and functional properties of this cell type. Therefore, we propose that these sea urchin exocrine cells are homologous to the well-known mammalian pancreatic acinar cells and thus we trace the origin of this particular cell type to the time of deuterostome diversification. Overall, our approach allows a thorough characterization of a complex cell type and shows how both the transcriptomic and morphological information contribute to disentangling the evolution of cell types and organs such as the pancreatic cells and pancreas. |
| first_indexed | 2024-04-13T02:22:33Z |
| format | Article |
| id | doaj.art-f6fd2b9f62b74c4baf7f0fcdf90e5182 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-04-13T02:22:33Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-f6fd2b9f62b74c4baf7f0fcdf90e51822022-12-22T03:06:55ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-08-011010.3389/fcell.2022.991664991664Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchinsPeriklis Paganos0Paolo Ronchi1Jil Carl2Giulia Mizzon3Pedro Martinez4Pedro Martinez5Giovanna Benvenuto6Maria Ina Arnone7Stazione Zoologica Anton Dohrn (SZN), Naples, ItalyEuropean Molecular Biology Laboratory (EMBL), Heidelberg, GermanyEuropean Molecular Biology Laboratory (EMBL), Heidelberg, GermanyEuropean Molecular Biology Laboratory (EMBL), Heidelberg, GermanyInstitut Català de Recerca i Estudis Avancats (ICREA), Barcelona, SpainGenetics Department, University of Barcelona, Barcelona, SpainStazione Zoologica Anton Dohrn (SZN), Naples, ItalyStazione Zoologica Anton Dohrn (SZN), Naples, ItalyThe identity and function of a given cell type relies on the differential expression of gene batteries that promote diverse phenotypes and functional specificities. Therefore, the identification of the molecular and morphological fingerprints of cell types across taxa is essential for untangling their evolution. Here we use a multidisciplinary approach to identify the molecular and morphological features of an exocrine, pancreas-like cell type harbored within the sea urchin larval gut. Using single cell transcriptomics, we identify various cell populations with a pancreatic-like molecular fingerprint that are enriched within the S. purpuratus larva digestive tract. Among these, in the region where they reside, the midgut/stomach domain, we find that populations of exocrine pancreas-like cells have a unique regulatory wiring distinct from the rest the of the cell types of the same region. Furthermore, Serial Block-face scanning Electron Microscopy (SBEM) of the exocrine cells shows that this reported molecular diversity is associated to distinct morphological features that reflect the physiological and functional properties of this cell type. Therefore, we propose that these sea urchin exocrine cells are homologous to the well-known mammalian pancreatic acinar cells and thus we trace the origin of this particular cell type to the time of deuterostome diversification. Overall, our approach allows a thorough characterization of a complex cell type and shows how both the transcriptomic and morphological information contribute to disentangling the evolution of cell types and organs such as the pancreatic cells and pancreas.https://www.frontiersin.org/articles/10.3389/fcell.2022.991664/fullsea urchinpancreasacinar cellsmorphologyevolution of cell typesscRNAseq |
| spellingShingle | Periklis Paganos Paolo Ronchi Jil Carl Giulia Mizzon Pedro Martinez Pedro Martinez Giovanna Benvenuto Maria Ina Arnone Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins Frontiers in Cell and Developmental Biology sea urchin pancreas acinar cells morphology evolution of cell types scRNAseq |
| title | Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins |
| title_full | Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins |
| title_fullStr | Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins |
| title_full_unstemmed | Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins |
| title_short | Integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar-like cells in sea urchins |
| title_sort | integrating single cell transcriptomics and volume electron microscopy confirms the presence of pancreatic acinar like cells in sea urchins |
| topic | sea urchin pancreas acinar cells morphology evolution of cell types scRNAseq |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2022.991664/full |
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