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My group is interested in understanding the evolution of the cells and molecules that regulate the balance between nutrient availability, growth and reproduction in animals. We use the sea anemone Nematostella vectensis (Cnidaria, Anthozoa) as a main model organism. In addition, the hydrozoan Clytia hemisphaerica and the scyphozoan Aurelia aurita are kept for comparative studies between the major cnidarian phyla.
Coordinating feeding, growing and reproducing is crucial for every animal’s development and survival. Nutrient homeostasis controls the uptake and storage of nutrients when food resources are available, and regulates the release of nutrients from storage tissue (e.g. fat depots) during times of higher needs or fasting. It is also important that animals restrict growth and reproduction to times when conditions are favourable. Thus, during the early evolution of multicellular animals, signalling systems must have evolved between cells and tissues to coordinate food supplies, metabolic demands, growth and reproduction. These systems were major drivers of animal body plan evolution. The evolution of organs with high energetic demands such as brains or muscles was relying on the capabilities to process large amounts of food and store excess nutrients. Numerous studies on bilaterian model organisms such as vertebrates, flies or nematodes have uncovered a complex interplay of diverse endocrine signals that coordinate nutrient and growth homeostasis between organs and tissues such as the brain, gut, fat cells, muscles or liver via the circulatory system. How the inter-cellular coordination between these cell types and organs has occurred during early animal evolution is currently unknown. Answering this question is however crucial to understand the gradual formation of the highly complex networks in flies or humans from simpler states.
Our main interests concentrate on the following questions:
- What is the molecular, cellular and developmental basis of nutrient uptake and release in sea anemones?
- How is feeding, fasting, growth and reproduction connected and controlled on the molecular, physiological and tissue level in sea anemones?
- How do the cell types and tissues involved in controlling nutrient homeostasis relate to well-described cell types and organs in bilaterian animals (e.g. pancreas, liver or adipocytes)?
Currently, my lab focuses on two aspects of nutrient homeostasis:
- The role of nutrients and feeding for juvenile growth
- The nutritional regulation of oogenesis
The cnidarian Nematostella vectensis (Anthozoa) is used as model organism as it offers a number of conceptual and technical advantages. Its simple body plan consists of only two cell layers and lacks highly specialised tissues such as a centralised nervous system or a circulatory system. In comparison to the more complex bilaterian animals, anthozoans thus provide a much simpler organismal framework. The molecular mechanisms and cellular interactions that coordinate nutrient and growth homeostasis might therefore be simpler and easier to disentangle than in most complex bilaterians. In addition, anthozoans appear to have evolved slowly both on the morphological (similar body plans) and genomic (ancestral gene content and genomic organisation) levels. Thus, the organismal simplicity might still represent an ancestral situation in many ways. Together, these features help reconstructing the molecular and cellular basis of how nutrient availability, growth and reproduction became coordinated during the evolution of complex multicellular animals.
Technically, we can combine a large set of molecular and genetic techniques recently established for Nematostella (e.g. CRISPR, microinjection of Morpholino oligonucleotides or mRNA, transgenic drivers and constructs) with more classical morphological or physiological methods (e.g. nutrient uptake, ultrastructure). We also benefit from a relatively large set of genomic, transcriptomic and epigenetic resources available for Nematostella.
Integration and comparison of the resulting data with the wealth of available data from bilaterian model organisms (e.g. vertebrates, Drosophila or C. elegans) will allow drawing a consistent, well-founded and potentially new picture of the evolution of animal nutrient and growth homeostasis. It will also help us understanding how the highly complex endocrine systems evolved from more simple ones during animal evolution. Finally, the simplicity of N. vectensis as research organism could unveil new and conserved players in controlling nutrient uptake and release that have so far remained undiscovered in bilaterians due to the high complexity and interconnectivity of the systems.
- 2019. A non-bilaterian perspective on the development and evolution of animal digestive systems. Cell and Tissue Research. 377: 321-339. doi: 10.1007/s00441-019-03075-x
- 2018. Cnidarian Cell Type Diversity and Regulation Revealed by Whole-Organism Single-Cell RNA-Seq. Cell. 173: 1520-1534.e20. doi: 10.1016/j.cell.2018.05.019
- 2017. Bud detachment in hydra requires activation of fibroblast growth factor receptor and a Rho–ROCK–myosin II signaling pathway to ensure formation of a basal constriction. Developmental Dynamics. 246: 502-516. doi: 10.1002/dvdy.24508
- 2017. Gut-like ectodermal tissue in a sea anemone challenges germ layer homology. Nature Ecology and Evolution. 1: 1535-1542. doi: 10.1038/s41559-017-0285-5
- 2016. The evolutionary origin of bilaterian smooth and striated myocytes. eLIFE. 5. doi: 10.7554/eLife.19607
I have been interested in diverse aspects of animal evolutionary development throughout my scientific career. During my PhD in the lab of Detlev Arendt at EMBL Heidelberg, I have worked on the morphogenesis and molecular sub-regionalisation of the nervous system in the polychaete annelid Platynereis dumerilii using 4D microscopy (PNAS, 2007) and comparative gene expression (e.g. Evol Dev, 2011; EvoDevo, 2010; Cell, 2007).
My postdoc work with Ulrich Technau, started at the Sars Centre in 2007 and continued at the University of Vienna from 2008, involved elucidating the evolutionary origin of germ layers and muscle cells. One part of the work used a broad phylogenomic comparison and cross-species comparative expression analysis of muscle components, and concluded that striated muscles evolved independently in jellyfish and bilaterian animals (e.g. vertebrates, flies)(Nature, 2012). In a second project, I studied the homology of cnidarian and bilaterian germ layers by comparing the origin of typical 'endodermal' (e.g. digestive enzyme-secreting exocrine cells) and 'mesodermal' (e.g. muscle, somatic gonad) cell types between the triploblastic bilaterians, and the diploblastic sea anemone Nematostella vectensis. This work challenged the long-held view that endoderm of cnidarians and bilaterians are homologous, and instead proposed a revised homology of germ layers (Nature Ecology and Evolution, 2017).
After a short time as independent researcher and tenure-track university assisstant at the University of Vienna, I started my lab at the Sars Centre in August 2015. My lab's interests are focussed on the evolution of the cells and molecules balancing nutrient availabilitiy, growth and reproduction using the sea anemone Nematostella vectensis as main research organism.