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The genome of the colonial hydroid Hydractinia reveals their stem cells utilize a toolkit of evolutionarily shared genes with all animals

Christine E. Schnitzler, E. Sally Chang, Justin Waletich, Gonzalo Quiroga-Artigas, Wai Yee Wong, Anh-Dao Nguyen, Sofia N. Barreira, Liam Doonan, Paul Gonzalez, Sergey Koren, James M. Gahan, Steven M. Sanders, Brian Bradshaw, Timothy Q. DuBuc, Febrimarsa, Danielle de Jong, Eric P. Nawrocki, Alexandra Larson, Samantha Klasfeld, Sebastian G. Gornik, R. Travis Moreland, Tyra G. Wolfsberg, Adam M. Phillippy, James C. Mullikin, Oleg Simakov, Paulyn Cartwright, Matthew Nicotra, Uri Frank, Andreas D. Baxevanis

Preprint posted on 27 August 2023 https://www.biorxiv.org/content/10.1101/2023.08.25.554815v1.full#ref-56

New genomes, old tricks! 🧬 @christyschnitz and team sequence the genomes of H. symbiolongicarpus and H. echinata to reveal a surprising enrichment of i-cell marker genes across animal species

Selected by Isabella Cisneros

Background:

When you hear Hydractinia, you may think instead of its more well-known freshwater counterpart, Hydra. While these organisms bear similar names, however, it is their differences that are key for understanding processes like regeneration. For the unfamiliar, Hydractinia is a colonial cnidarian typically found on the backs of hermit crab shells in nature. Hydractinia colonies are composed of three types of polyps—feeding polyps, sexual polyps, and defensive polyps—growing from a tissue known as the stolonal mat [1].

You may be wondering what about Hydractinia makes it a model with so much potential. Experimentally speaking, Hydractinia colonies are easy to culture, lend themselves to imaging experiments due to their optically translucent nature, and allow for transgenesis and gene knockdown [2]. Hydractinia also possesses a population of adult pluripotent stem cells termed “i-cells” that underlie their remarkable regenerative abilities, which have been characterized in previous reports [3, 4]. Unlike Hydra, which has three self-renewing stem cell lineages, these stem cells belong to a single self-renewing lineage, making them a particularly attractive target for studies of stem cell and regeneration biology [3, 5]. Hydractinia also lends itself to studies of allorecognition [6]. Despite all this, the absence of a complete genome has hindered the further establishment of Hydractinia as a model organism.

In this preprint, the authors sequenced the genomes of sister species H. symbiolongicarpus and H. echinata and produced the first single-cell atlas for H. symbiolongicarpus. In doing so, the authors further establish Hydractinia as a model organism for regenerative and allorecognition studies, paving the way for future studies to come.

 

Main Findings:

Putting H. symbiolongicarpus and H. echinata into evolutionary context

Once the authors had assembled and annotated both Hydractinia genomes—and completed some initial analyses on phylogenetics, divergence, and synteny—they proceeded to analyze lineage specificity and evolutionary novelty in Hydractinia. The contribution of taxon-restricted and shared ancestral gene families to cnidarian-specific cell types was analyzed using Orthofinder2, a comparative genomics software. The results showed that 26% of the orthogroups inferred by Orthofinder were cnidarian-specific, which, when compared to the 24% of bilaterian-specific orthogroups found from sampled bilaterian species, seems to indicate that evolutionary novelty in cnidarians is equal to that found in bilaterians. Further analysis of whether genes assigned to orthogroups were species-specific, phylum-specific, or metazoan-specific revealed that Hydractinia possesses the highest number of cnidarian-specific genes out of all the 16 cnidarians included in the study. Additionally, a search using the protein alignment software DIAMOND showed that the majority of unassigned Hydractinia genes had no match in the NCBI database, indicating that these Hydractinia genomes have a significant amount of evolutionary novel genes.

Single cell transcriptomics and the creation of a robust cell-type atlas for H. symbiolongicarpus

Following additional analysis of genome characteristics, the authors performed a single cell transcriptome analysis of a wild-type H. symbiolongicarpus strain using a 10X Genomics platform. Downstream analyses of the sequencing data yielded heatmaps and UMAP plots that allowed the authors to visualize cell cluster data. After additional filtering, 18 cell clusters were generated and subsequently classified as putative cell types or cell states. Of these, the authors selected seven clusters for validation using fluorescence in situ hybridization to visualize two previously published gene markers and five novel cell-type markers. All the gene markers tested showed the expected expression pattern, marking the first step towards defining all major cell types in Hydractinia.

Orthology analyses indicate that Hydractinia i-cell markers are widely shared across animals

After generating the single cell atlas, the authors decided to probe the evolutionary profile of marker genes across the 18 clusters using OrthoFinder2. Interestingly, they found that i-cell, progenitor, and early spermatogonia clusters are defined primarily by shared genes, not lineage-specific genes. To further analyze the nature of the i-cell cluster, the authors subsequently plotted how many of the animal species included in the orthology analysis shared the i-cell marker genes identified. Surprisingly, the authors found that the majority of the 317 i-cell marker genes were present in 40 or more species, leading them to reason that Hydractinia’s stem cells may be utilizing a shared gene toolkit found in nearly all animals.

 

Why I Chose This Preprint:

This study is impressive both in its scope and its comprehensiveness. The authors tackle not one, but two Hydractinia genomes, characterizing a wide array of features inherent to these genomes. They use the generated data to construct a comparative evolutionary framework both within Cnidaria and beyond it. I was surprised by the sheer amount of data generated by the authors, as well as their deft handling and unpacking of it throughout the preprint. I also found their results regarding the widespread presence of i-cell marker genes incredibly interesting and promising for future study. Given Hydractinia’s unique stem cell lineage, it will be a particularly effective model for understanding the extent of this toolkit. Now, with these genomes in hand, it will be possible to further establish this model organism and bridge discoveries across different animal species.

 

Questions For The Authors:

  1. How do you reconcile the large number of shared i-cell marker genes with the higher proportions of phylum-specific and cnidarian specific genes in the H. symbiolongicarpus genome?
  2. Towards the end of the preprint, you claim that it remains unclear whether other animals share the same toolkit of genes, or whether these toolkits are instead partially overlapping. While further studies will be necessary to determine this, at this stage, what do you anticipate to be the case?
  3. Given the different evolutionary trajectories that H. symbiolongicarpus and H. echinata have followed since divergence, what kinds of studies would be better suited for each species, if any? What could be gained by using both species in a comparative framework?

 

References

[1] Frank, U., Nicotra, M.L. & Schnitzler, C.E. The colonial cnidarian HydractiniaEvoDevo 11, 7 (2020). https://doi.org/10.1186/s13227-020-00151-0

[2] Plickert, G., Jacoby, V., Frank, U., Müller, W. A., & Mokady, O. Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Developmental Biology298(2), 368-378 (2006). https://doi.org/10.1016/j.ydbio.2006.06.043

[3] Varley Á, Horkan HR, McMahon ET, Krasovec G, Frank U. Pluripotent, germ cell competent adult stem cells underlie cnidarian regenerative ability and clonal growth. Curr Biol., 33(10): 1883-1892.e3 (2023). doi: 10.1016/j.cub.2023.03.039.

[4] Bradshaw, B., Thompson, K., Frank, U. Distinct mechanisms underlie oral vs aboral regeneration in the cnidarian Hydractinia echinata. eLife 4:e05506 (2015). https://doi.org/10.7554/eLife.05506

[5] Bosch, T.C.G., Anton-Erxleben, F., Hemmrich, G. and Khalturin, K. The Hydra polyp: Nothing but an active stem cell community. Development, Growth & Differentiation, 52: 15-25 (2010). https://doi.org/10.1111/j.1440-169X.2009.01143.x

[6] Nicotra, M.L. The Hydractinia allorecognition system. Immunogenetics 74, 27–34 (2022). https://doi.org/10.1007/s00251-021-01233-6

Tags: cell atlas, cnidarian, genome, stem cells, transcriptomics

Posted on: 19 September 2023

doi: https://doi.org/10.1242/prelights.35599

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