The genome of the colonial hydroid Hydractinia reveals their stem cells utilize a toolkit of evolutionarily shared genes with all animals
Posted on: 19 September 2023 , updated on: 31 July 2024
Preprint posted on 27 August 2023
Article now published in Genome Research at http://dx.doi.org/10.1101/gr.278382.123
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
Categories: bioinformatics, developmental biology, evolutionary biology, genomics
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:
- 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?
- 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?
- 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 Hydractinia. EvoDevo 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 Biology, 298(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
doi: https://doi.org/10.1242/prelights.35599
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(No Ratings Yet)Author's response
Dr Christine Schnitzler shared
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?
We took the entire genome and ran an orthology clustering of all predicted proteins from 49 other animals, including 16 cnidarians. We put them into bins once we got the clusters back. Are these genes in a “multi-species orthogroup?” That means they group with genes from animals outside of cnidarians, so they’re shared more widely. A lot of the other categories were cnidarian-specific.
This graph shows just the cnidarians and a few other animal outgroups. Those two [asterisked] red bars are further out than all the other cnidarians — they had the highest proportion of genes in their genome that were specific to their phylum.
If you apply that same clustering to the most highly expressed genes that are specific to just the i-cells, we found that i-cell genes are mostly shared with other animals (that was the title of the paper).
They’re undifferentiated cells that have to use basic cell characteristics — cell cycle genes, genes that help with proliferation, genes that are involved in maintaining stemness — and these are universal things that all animals have developed and retained throughout evolution.
That does not mean that stem cells of Hydractinia are exactly homologous to the stem cells of other animals. Cell types can evolve very quickly, but the underlying genes that make stem cells stem cells are very highly conserved.
There are a lot of cnidarian-specific genes in their genomes. It’s just in their stem cells, they’re not using those very much. But when you think about stem cells, they’re not really unique to cnidarians. All animals have some type of a stem cell — that’s just how it works.
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?
It’s very hard to relate cell types and say they have a shared evolutionary origin of the cell type. If you look at stem cells in Hydractinia and then look at stem cells in planarians, they have a lot of shared characteristics. But what about all the animals in between? Where did their stem cells go? I think that’s a very interesting question.
I think getting down to this core level of genes and gene regulatory networks that are controlling these types of cells, to me, might be more interesting and more informative from an evolutionary perspective than trying to absolutely say this cell type first arose at some point and then shifted. It’s not really about the cell types. It’s more about the core genes that are involved and finding out their function. And it’s really hard. I think the only way really is to drill down on function within several animals and then try to see if they relate to each other.
It’s good to look at informative positions on the tree, as a lot of people try to do, and try to gain as much insight as you can from looking at those different places. I don’t think there’s going to be 100% overlap. But I think there will be themes that emerge — categories of genes that may be similar. You could group them by orthology, but maybe not exactly by BLAST.
It’s a question for the future. I think people are trying to tackle it, but it’s going to take more than these genome-wide approaches. We’ll have to go back to the lab and do functional testing to get at those questions.
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?
Most people have dropped H. echinata as a research organism. It’s got a bigger genome that’s not as well assembled. And no one’s maintaining them in the lab, anymore. They’re just harder to keep in culture long term. There may be some ecological and other questions that might be more interesting with echinata, and it would be cool if someone picks it up now that the genome is available.
On the other hand, H. symbiolongicarpus just grows and grows and grows indefinitely. After years and years of being in culture, we can still get them to spawn on a weekly basis and get tons of embryos. It also has a smaller genome that ended up with a better assembly.
So for us, the path forward is symbiolongicarpus. Now we can talk and really understand each other when we’re talking about a particular gene or a particular process. Now we have this resource. It’s a starting point.
One interesting thing to think about is what is unique about Hydractinia biology? I like Hydractinia because it is different. It’s colonial with a polymorphism of polyp types. We have feeding polyps, sexual polyps, defensive polyps. Because we have this diversity just within a single colony, there are a lot more questions to ask. It’s a different type of development, a different kind of asexual reproduction.
The other thing that I think is super cool is its lifecycle. It’s a hydrozoan that has lost the medusa stage. So there’s no jellyfish stage. Its next closest sister group is Podocoryna carnea, which does have a polyp and a medusa stage. That genome is being sequenced now. So when we have these two genomes — Podocoryna and Hydractinia — you can now start to understand the difference between a hydrozoan genome that produces the medusa jellyfish and the genome that doesn’t. I think some of these comparative studies with new genomes are really, really exciting. And I think with unlimited resources, we would have perfectly assembled genomes for those two groups and start doing more experiments to try to understand the unique biology of Hydractinia.
One thing our paper does not really focus on is regeneration. Hydractinia symbiolongicarpus is a model of regeneration. There’s a huge amount of knowledge we can learn by studying regeneration in this animal. There’s been some seminal ground laying papers about regeneration in this model, but doing updated studies, which we have some data, hopefully soon we can update and talk more about how this animal achieves its amazing regenerative abilities.
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