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Atlas of the Neuromuscular System in the Trachymedusa Aglantha Digitale: Insights from the Advanced Hydrozoan

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Atlas of the Neuromuscular System in the Trachymedusa Aglantha Digitale: Insights from the Advanced Hydrozoan bioRxiv preprint doi: https://doi.org/10.1101/772418; this version posted September 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Atlas of the Neuromuscular System in the Trachymedusa Aglantha digitale: Insights from the advanced hydrozoan Tigran P. Norekian1,2,3, Leonid L. Moroz1, 4* 1Whitney Laboratory for Marine Biosciences, University of Florida, St. Augustine, FL, 32080, USA; 2Friday Harbor Laboratories, University of Washington, Friday Harbor, WA, USA; 3Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow 117485, Russia; 4Departments of Neuroscience and McKnight Brain Institute, University of Florida, Gainesville, FL, 32610, USA. Keywords: Cnidarians, Nervous System, Muscle System, Sensory Cells, Nematocysts, Nematostella, Evolution; Figures: 18 *Corresponding author: Dr. Leonid L. Moroz The Whitney Laboratory; University of Florida; 9505 Ocean Shore Blvd. St. Augustine, FL 32080, USA; Phone: +1-904-461-4006; Fax: +1-904-461-9052; email: [email protected] Grant Acknowledgments: This work was supported by the National Science Foundation (grants 1146575, 1557923, 1548121 and 1645219). ABSTRACT Cnidaria is the sister taxon to bilaterian animals, and therefore, represents a key reference lineage to understand early origins and evolution of the neural systems. The hydromedusa Aglantha digitale is arguably the best electrophysiologically studied jellyfish because of its system of giant axons and unique fast swimming/escape behaviors. Here, using a combination of scanning electron microscopy and immunohistochemistry together with phalloidin labeling, we systematically characterize both neural and muscular systems in Aglantha, summarizing and expanding further the previous knowledge on the microscopic neuroanatomy of this crucial reference species. We found that the majority, if not all (~2500) neurons, that are labeled by FMRFamide antibody are different from those revealed by anti-α-tubulin immunostaining, making these two neuronal markers complementary to each other and, therefore, expanding the diversity of neural elements in Aglantha with two distinct neural subsystems. Our data uncovered the complex organization of neural networks forming a functional ‘annulus-type’ central nervous system with three subsets of giant axons, dozen subtypes of neurons, muscles and a variety of receptors fully integrated with epithelial conductive pathways supporting swimming, escape and feeding behaviors. The observed unique adaptations within the Aglantha lineage (including giant axons innervating striated muscles) strongly support an extensive and wide-spread parallel evolution of integrative and effector systems across Metazoa. bioRxiv preprint doi: https://doi.org/10.1101/772418; this version posted September 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 INTRODUCTION cnidarian neuromuscular systems are focused on two reference species (Leitz, The phylum Cnidaria (jellyfishes, 2016): Hydra (a highly specialized polyps, sea anemones, and corals) is one freshwater hydrozoan, which lost the of the five early branching metazoan medusa stage) and Nematostella (an lineages. Together with Ctenophores and anthozoan, with a primary absence of Bilaterians, they were united within a medusas in its life cycle). Unfortunately, single group of Eumetazoa – the taxon Mesdusozoa received less attention of combining all animals with true neural neuroscientists, despite substantial and and muscular systems, whereas sponges widespread occurrences of jellyfishes and placozoans represent the lineages word-wide (see reviews in (Satterlie and with a primary absence of neurons and Nolen, 2001; Satterlie, 2002; Mackie, muscles (Kozloff, 1990; Brusca and 2004; Satterlie, 2011; Steinmetz et al., Brusca, 2003; Nielsen, 2012). Recent 2012; Satterlie, 2015b; a)). phylogenomic studies consistently place Among jellyfishes, there is a cnidarians as the sister group to bilaterian distinct family of Rhopalonematidae animals (Whelan et al., 2015; Arcila et (Trachylina/Hydrozoa), which al., 2017; Simion et al., 2017; Whelan et completely lost their polyp stages and al., 2017). Cnidaria and Bilateria united developed multiple adaptations to as the distinct clade of animals with (meso)pelagic life. The most accessible nervous systems, which possible share a species in this family is Aglantha digitale common origin. In contrast, ctenophores – the Northern jellyfish, predominantly might evolve neural and muscular living in deep waters (50-200 m). systems independently from the common Aglantha frequently reaches surfaces due ancestor of Cnidaria+Bilateria (Moroz, to mixing currents or upwelling in spring- 2014; Moroz et al., 2014; Moroz, 2015; summer time around the San Guam Moroz and Kohn, 2016). Thus, Archipelago (Northwest Pacific). Eumetazoa could be a polyphyletic taxon, Aglantha digitale is well-known and Cnidaria is a key reference group to for its fast swimming and escape understand the origin of integrative response and differ from most other systems in bilaterians. However, jellyfishes in having three subsets of giant cnidarian neuromuscular systems are axons (motor axons in the bell, ring axon, highly diverse in their structures and and tentacle axons) - a perfect example forms, which reflect enormous of convergent evolution of conductive biodiversity within this group (Bullock systems mediating synchronous and Horridge, 1965; Spencer and Arkett, coordinating contractions of the body 1984; Mackie, 1990; Satterlie, 2002; wall and tentacles for jet-like locomotion 2011; Steinmetz et al., 2012; Satterlie, (Singla, 1978; Roberts and Mackie, 1980; 2015b; Leitz, 2016). Weber et al., 1982). Surprisingly, the Most detailed recent studies of very same giant axons mediate both fast bioRxiv preprint doi: https://doi.org/10.1101/772418; this version posted September 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. (escape) and slow (fishing) swimming by electron microscopy (SEM), fluorescent utilizing two different spikes, with immunocytochemistry for labeling neural sodium and calcium ionic mechanisms elements, and phalloidin for labeling respectively (Mackie and Meech, 1985; muscle fibers, we present and summarize Mackie and Meech, 1995b; a; Meech, the organization of the neuromuscular 2015). systems in Aglantha, which provide a Twelve functional neural and two foundation to expand our understanding conductive epithelial systems were of this unique system in the future with described in Aglantha, leading to the modern molecular tools. suggestion that Aglantha possesses a functional analog of the central nervous 2 MATERIALS AND METHODS system, in the form of annulus rather than a compact ganglion (summarized by 2.1 Animals (Mackie, 2004)). Aglantha independently Adult specimens of Aglantha (from some bilaterians and ctenophores) digitale (the family Rhopalonematidae) evolved striated muscles as an additional were collected from the breakwater and adaptation to fast jet-propulsion held in 1-gallon glass jars in the large swimming. tanks with constantly circulating In the past, Aglantha has been seawater at 10o - 12o C. Experiments were studied intensively by several researchers carried out at Friday Harbor Laboratories, both neurophysiologically and the University of Washington in the structurally (Singla, 1978; Donaldson et spring-summer seasons of 2016-2019. al., 1980; Mackie, 1980; Roberts and Mackie, 1980; Weber et al., 1982; Singla, 2.2 Scanning Electron Microscopy 1983; Kerfoot et al., 1985; Mackie and (SEM) Meech, 1985; Arkett et al., 1988; Meech Animals were fixed whole in and Mackie, 1993b; a; Mackie and 2.5% glutaraldehyde in 0.1 M cacodylic- Meech, 1995b; a; Meech and Mackie, buffered saline (pH=7.6) for 4 hours at 1995; Mackie and Meech, 2000; Mackie room temperature and washed for a few et al., 2003; Mackie, 2004; Mackie and hours in 0.1 M cacodylic acid buffer. Meech, 2008). However, little is known Larger animals, more than 1 cm in about the neurotransmitter organization diameter, were then dissected into a few in Aglantha. For example, it was reported smaller pieces, while small animals were that nitric oxide signaling controls processed as whole mounts. For swimming, possibly via nitrergic sensory secondary fixation, we used 2% osmium neurons in tentacles (Moroz et al., 2004), tetroxide in 0.1 M cacodylic buffer for 2 and peptidergic innervation of hours at room temperature. Tissues were feeding/receptive systems was also then rinsed several times with distilled proposed (Mackie et al., 1985). water, dehydrated in ethanol (series of Here, by utilizing scanning 20-minute incubations in 30%, 50%, 70%, 90% and 100% ethanol) and placed bioRxiv preprint doi: https://doi.org/10.1101/772418; this version posted September 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available
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