Uncovering the role of taxonomically restricted genes in the basal metazoan Hydra
Final Report Abstract
Up to 40% of the genes in the genome of any animal species are represented by non-conserved, taxonomically restricted genes (TRGs). These genes show no homology to other genes outside that species or clade and are therefore restricted to a species, genus or phylum. The freshwater polyp Hydra represents a powerful model to dissect TRGs at the functional level due to its phylogenetic position, experimental accessibility, and remarkably high abundance of TRGs in its genome. The aim of this project was to gain insight into the developmental role of TRGs in Hydra. First, I generated a high quality genome assembly of H. vulgaris AEP to complement the recently published reference genome. This will facilitate comparative analyses and allow a detailed understanding of the TRG repertoire and their evolutionary dynamics in Hydra. Second, my systematic genome-wide survey identified numerous individual TRGs and their families in Hydra. In silico analysis using advanced tools like machine learning revealed significant structural and functional diversity among these genes. Functional analysis using transgenic Hydra revealed that some TRGs play critical roles in neuronal maturation and individuation. This highlights the importance of genomic novelty in cell type development and evolution. My findings provide new insights into how TRGs are embedded in gene regulatory networks and complement the machinery of conserved developmental genes. Further, I performed a comprehensive analysis of antimicrobial peptide (AMP)-encoding TRGs in Hydra and uncovered their remarkable expansion and complexity. My findings provide evidence for the evolutionary importance of TRGs in shaping species-specific microbiomes and maintaining holobiont homeostasis. The isolation of promoters driving the expression of neuron-specific TRGs allowed the generation of unique transgenic Hydra lines expressing reporters such as GFP and GCaMP6. These lines allowed detailed analysis of the architecture and activity of the Hydra nervous system. These resources, already available to the research community, will support ongoing and future studies of Hydra nervous system development, function, and evolution. This project has opened up several new research lines. In particular, the high evolutionary dynamics observed in some TRG families, especially those encoding AMPs, suggest ongoing adaptation processes that warrant further investigation. Comparison of complete genomes from different Hydra strains revealed substantial copy number variation in TRG families. Future research will focus on linking genome dynamics with life histories and ecological adaptations within the Hydra lineage. Overall, my project significantly advances our understanding of TRGs in Hydra, provides critical insights into their structural and functional roles, and establishes fundamental tools and frameworks for further exploration of the TRGs’ developmental role.
Publications
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The Role of DNA Methylation in Genome Defense in Cnidaria and Other Invertebrates. Molecular Biology and Evolution, 39(2).
Ying, Hua; Hayward, David C.; Klimovich, Alexander; Bosch, Thomas C. G.; Baldassarre, Laura; Neeman, Teresa; Forêt, Sylvain; Huttley, Gavin; Reitzel, Adam M.; Fraune, Sebastian; Ball, Eldon E. & Miller, David J.
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Multiple neuronal populations control the eating behavior in Hydra and are responsive to microbial signals. Current Biology, 33(24), 5288-5303.e6.
Giez, Christoph; Pinkle, Denis; Giencke, Yan; Wittlieb, Jörg; Herbst, Eva; Spratte, Tobias; Lachnit, Tim; Klimovich, Alexander; Selhuber-Unkel, Christine & Bosch, Thomas C.G.
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Spontaneous body wall contractions stabilize the fluid microenvironment that shapes host–microbe associations. eLife, 12.
Nawroth, Janna C.; Giez, Christoph; Klimovich, Alexander; Kanso, Eva & Bosch, Thomas CG
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Spontaneously occurring tumors in different wild-derived strains of hydra. Scientific Reports, 13(1).
Boutry, Justine; Buysse, Marie; Tissot, Sophie; Cazevielle, Chantal; Hamede, Rodrigo; Dujon, Antoine M.; Ujvari, Beata; Giraudeau, Mathieu; Klimovich, Alexander; Thomas, Frédéric & Tökölyi, Jácint
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Genetic interference with HvNotch provides new insights into the role of the Notch-signalling pathway for developmental pattern formation in Hydra. Scientific Reports, 14(1).
Pan, Qin; Mercker, Moritz; Klimovich, Alexander; Wittlieb, Jörg; Marciniak-Czochra, Anna & Böttger, Angelika
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Novel technologies uncover novel ‘anti’-microbial peptides in Hydra shaping the species-specific microbiome. Philosophical Transactions of the Royal Society B: Biological Sciences, 379.
Klimovich, Alexander & Bosch, Thomas C. G.
