Chapter Eleven - Animal development in the microbial world: The power of experimental model systems

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Abstract

The development of powerful model systems has been a critical strategy for understanding the mechanisms underlying the progression of an animal through its ontogeny. Here we provide two examples that allow deep and mechanistic insight into the development of specific animal systems. Species of the cnidarian genus Hydra have provided excellent models for studying host-microbe interactions and how metaorganisms function in vivo. Studies of the Hawaiian bobtail squid Euprymna scolopes and its luminous bacterial partner Vibrio fischeri have been used for over 30 years to understand the impact of a broad array of levels, from ecology to genomics, on the development and persistence of symbiosis. These examples provide an integrated perspective of how developmental processes work and evolve within the context of a microbial world, a new view that opens vast horizons for developmental biology research. The Hydra and the squid systems also lend an example of how profound insights can be discovered by taking advantage of the “experiments” that evolution had done in shaping conserved developmental processes.

Section snippets

Models systems as a strategy for understanding conserved features of complex processes like development

“For a large number of problems there will be some animal of choice on which it can be most conveniently studied … I am afraid that most of them are unknown … Zoologists need to find them and lay their hands on them” (Krogh, 1929). Even before this insight by Krogh and in the years to follow, much has been learned about development through the study of animal models, a small set of diverse metazoans that have particular advantages for laboratory research. Research with model systems (Fig. 1)

Hydra: A model for host-microbe interactions—And a window into early animal life

The freshwater polyp Hydra (Fig. 2A and B) is an excellent model for studying host-microbe interactions and how metaorganisms function in vivo (Bosch, 2013, Bosch, 2014; Klimovich & Bosch, 2018; Schröder & Bosch, 2016). In Hydra's simple tube-like body structure, the single layer of ectodermal epithelial cells covered by a multilayered glycocalyx represents a physical barrier toward the environment, whereas a single layer of endodermal epithelial cells separates the body from the content of the

The binary light organ squid-vibrio model sheds light on basic mechanisms of symbiosis development

The association of the Hawaiian bobtail squid Euprymna scolopes and the luminous vibrio bacterium Vibrio fischeri has been studied for over 30 years (for companion reviews on host and symbiont see: Nyholm & McFall-Ngai, 2020 and Stabb, Visick, & Ruby, 2020 Nature Reviews Microbiology). At the time of this writing, 18 labs with a principal focus on the squid-vibrio system have opened in 14 states or US territories. This natural model symbiosis has been used to identify and characterize the

Conclusion

Biology is a complex science at every level. As such, it demands mechanisms by which to make sense of and find patterns in its diversity. Since the advent of next-generation sequencing, biologists have become increasingly aware that animals are typically complex assemblages of organisms, i.e., the host and its associated microbial partners. To understand their development, we will need to bring on all available models. In an insightful essay on the nature of models [//sites.google.com/a/ncsu.edu/emily-griffiths/whatisamodel.pdf

Acknowledgments

We thank Scott Gilbert for the opportunity to contribute to this volume and for critically reading the manuscript. M.M.-N. is currently funded by National Institutes of Health (NIH) R37 AI50661 (to M.M.-N. and E.G. Ruby); NIH, Center for Biomedical Research Excellence P20 GM125508 (to M.M.-N. and E.G. Ruby); NIH R01 OD11024 and GM135254 (to E.G. Ruby and M.M.-N.); and a grant from the Gordon and Betty Moore Foundation (to A. Briegel, U. Leiden, M.M.-N., E.G. Ruby and A. Septer, U. North

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