Christine E. Schnitzler1,2, E. Sally Chang3,4, Justin Waletich1,2, Gonzalo Quiroga-Artigas1,2,5, Wai Yee Wong6, Anh-Dao Nguyen3, Sofia N. Barreira3, Liam B. Doonan7, Paul Gonzalez3, Sergey Koren3, James M. Gahan7,8, Steven M. Sanders9,10, Brian Bradshaw7, Timothy Q. DuBuc7,11, Febrimarsa7,12, Danielle de Jong1,2, Eric P. Nawrocki4, Alexandra Larson1, Samantha Klasfeld3, Sebastian G. Gornik7,13, R. Travis Moreland3, Tyra G. Wolfsberg3, Adam M. Phillippy3, James C. Mullikin3,14, Oleg Simakov6, Paulyn Cartwright15, Matthew Nicotra9,10, Uri Frank7 and Andreas D. Baxevanis3 1Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, Florida 32080, USA; 2Department of Biology, University of Florida, Gainesville, Florida 32611, USA; 3Division of Intramural Research, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA; 4National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20892, USA; 5Centre de Recherche en Biologie cellulaire de Montpellier (CRBM), Université de Montpellier, Centre National de la Recherche Scientifique, 34293 Montpellier CEDEX 05, France; 6Department for Neurosciences and Developmental Biology, University of Vienna, 1030 Vienna, Austria; 7Centre for Chromosome Biology, College of Science and Engineering, University of Galway, Galway H91 W2TY, Ireland; 8Department of Biochemistry, University of Oxford, Oxford OX1 3QU, United Kingdom; 9Department of Surgery, Thomas E. Starzl Transplantation Institute, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA; 10Pittsburgh Center for Evolutionary Biology and Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA; 11Department of Biology, Swarthmore College, Swarthmore, Pennsylvania 19081, USA; 12Pharmaceutical Biology Laboratory, Faculty of Pharmacy, Universitas Muhammadiyah Surakarta, Jawa Tengah 57169, Indonesia; 13Center for Organismal Studies, University of Heidelberg, 69117 Heidelberg, Germany; 14NIH Intramural Sequencing Center, Rockville, Maryland 20852, USA; 15Department of Evolution and Ecology, University of Kansas, Lawrence, Kansas 66045, USA Corresponding author: andymail.nih.gov Abstract

Hydractinia is a colonial marine hydroid that shows remarkable biological properties, including the capacity to regenerate its entire body throughout its lifetime, a process made possible by its adult migratory stem cells, known as i-cells. Here, we provide an in-depth characterization of the genomic structure and gene content of two Hydractinia species, Hydractinia symbiolongicarpus and Hydractinia echinata, placing them in a comparative evolutionary framework with other cnidarian genomes. We also generated and annotated a single-cell transcriptomic atlas for adult male H. symbiolongicarpus and identified cell-type markers for all major cell types, including key i-cell markers. Orthology analyses based on the markers revealed that Hydractinia’s i-cells are highly enriched in genes that are widely shared amongst animals, a striking finding given that Hydractinia has a higher proportion of phylum-specific genes than any of the other 41 animals in our orthology analysis. These results indicate that Hydractinia’s stem cells and early progenitor cells may use a toolkit shared with all animals, making it a promising model organism for future exploration of stem cell biology and regenerative medicine. The genomic and transcriptomic resources for Hydractinia presented here will enable further studies of their regenerative capacity, colonial morphology, and ability to distinguish self from nonself.

Footnotes

[Supplemental material is available for this article.]

Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.278382.123.

Freely available online through the Genome Research Open Access option.

Received August 25, 2023. Accepted March 7, 2024.