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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 Received: 11 September 2019 Revised: 17 November 2019 Accepted: 18 November 2019 DOI: 10.1002/cne.24821 RESEARCH ARTICLE 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, Florida Abstract 2Friday Harbor Laboratories, University of Cnidaria is the sister taxon to bilaterian animals, and therefore, represents a key refer- Washington, Friday Harbor, Washington ence lineage to understand early origins and evolution of the neural systems. The 3Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of hydromedusa Aglantha digitale is arguably the best electrophysiologically studied jelly- Sciences, Moscow, Russia fish because of its system of giant axons and unique fast swimming/escape behaviors. 4 Department of Neuroscience and McKnight Here, using a combination of scanning electron microscopy and immunohistochemistry Brain Institute, University of Florida, Gainesville, Florida together with phalloidin labeling, we systematically characterize both neural and mus- cular systems in Aglantha, summarizing and expanding further the previous knowledge Correspondence Leonid L. Moroz, The Whitney Laboratory, on the microscopic neuroanatomy of this crucial reference species. We found that the University of Florida, 9505 Ocean Shore Blvd., majority, if not all (~2,500) neurons, that are labeled by FMRFamide antibody are dif- St. Augustine, FL. Email: [email protected] ferent from those revealed by anti-α-tubulin immunostaining, making these two neuro- nal markers complementary to each other and, therefore, expanding the diversity of Funding information National Science Foundation, Grant/Award neural elements in Aglantha with two distinct neural subsystems. Our data uncovered Numbers: 1645219, 1548121, 1557923, the complex organization of neural networks forming a functional “annulus-type” cen- 1146575 tral nervous system with three subsets of giant axons, dozen subtypes of neurons, Peer Review muscles, and a variety of receptors fully integrated with epithelial conductive pathways The peer review history for this article is available at https://publons.com/publon/10. supporting swimming, escape and feeding behaviors. The observed unique adaptations 1002/cne.24821. 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. KEYWORDS cell atlas, Cnidaria, evolution, hydra, muscle system, nematocysts, Nematostella, nervous system, sensory cells 1 | INTRODUCTION Halanych, 2015). Cnidaria and Bilateria are united as the distinct clade of animals with nervous systems that possibly share a common origin. In The phylum Cnidaria (jellyfishes, polyps, sea anemones, and corals) is contrast, ctenophores might have evolved neural and muscular systems one of the five early branching metazoan lineages. Together with Cteno- independently from the common ancestor of Cnidaria+Bilateria (Moroz, phores and Bilaterians, they were united within a single group of 2014; Moroz, 2015; Moroz et al., 2014; Moroz & Kohn, 2016). Thus, Eumetazoa—the taxon combining all animals with true neural and mus- Eumetazoa could be a polyphyletic taxon, and Cnidaria is a key refer- cular systems, whereas sponges and placozoans represent the lineages ence group to understand the origin of integrative systems in bilaterians. with a primary absence of neurons and muscles (Brusca & Brusca, 2003; However, cnidarian neuromuscular systems are highly diverse in their Kozloff, 1990; Nielsen, 2012). Recent phylogenomic studies consistently structures and forms, which reflect enormous biodiversity within this place cnidarians as the sister group to bilaterian animals (Arcila et al., group (Bullock & Horridge, 1965; Leitz, 2016; Mackie, 1990; Satterlie, 2017; Simion et al., 2017; Whelan et al., 2017; Whelan, Kocot, Moroz, & 2002, 2011, 2015b; Spencer & Arkett, 1984; Steinmetz et al., 2012). J Comp Neurol. 2020;528:1231–1254. wileyonlinelibrary.com/journal/cne © 2019 Wiley Periodicals, Inc. 1231 1232 NOREKIAN AND MOROZ Most detailed recent studies of cnidarian neuromuscular sys- 2 | MATERIALS AND METHODS tems are focused on two reference species (Leitz, 2016): Hydra (a highly specialized freshwater hydrozoan, which lost the medusa 2.1 | Animals stage) and Nematostella (an anthozoan, with a primary absence of medusas in its life cycle). Unfortunately, Medusozoa received less Adult specimens of A. digitale Muller 1776 (family Rhopalonematidae) attention of neuroscientists, despite substantial and widespread were collected from the breakwater and held in 1-gal glass jars in the occurrences of jellyfishes word-wide (see reviews Satterlie & Nolen, large tanks with constantly circulating seawater at 10C–12C. Exper- 2001; Satterlie, 2002, 2011, 2015a, 2015b; Mackie, 2004; Stein- iments were carried out at Friday Harbor Laboratories, the University metz et al., 2012). of Washington in the spring–summer seasons of 2016–2019. Among jellyfishes, there is a distinct family of Rhopalonematidae (Trachylina/Hydrozoa), which completely lost their polyp stages and developed multiple adaptations to (meso)pelagic life. The most 2.2 | Scanning electron microscopy (SEM) accessible species in this family is Aglantha digitale—the Northern jellyfish, predominantly living in deep waters (50–200 m). Aglantha Prior to fixation, the animals were incubated for 30 min in 1:1 mixture frequently reaches surfaces due to mixing currents or upwelling in of 0.3 M MgCl2 and filtered seawater to relax the tissue. Then the ani- spring–summer time around the San Juan Archipelago (Northwest mals were fixed whole in 2.5% glutaraldehyde in 0.1 M cacodylic- Pacific). buffered saline (pH = 7.6) for 4 hr at room temperature and washed A. digitale is well-known for its fast swimming and escape for a few hours in 0.1 M cacodylic acid buffer. Larger animals, more response and differs from most other jellyfishes in having three sub- than 1 cm in diameter, were then dissected into a few smaller pieces, sets of giant axons (motor axons in the bell, ring axon, and tentacle while small animals were processed as whole mounts. For secondary axons)—a perfect example of convergent evolution of conductive sys- fixation, we used 2% osmium tetroxide in 0.1 M cacodylic buffer for tems mediating synchronous coordinating contractions of the body 2 hr at room temperature. Tissues were then rinsed several times with wall and tentacles for jet-like locomotion (Roberts & Mackie, 1980; distilled water, dehydrated in ethanol (series of 20-min incubations in Singla, 1978b; Weber, Singla, & Kerfoot, 1982). Surprisingly, the very 30%, 50%, 70%, 90%, and 100% ethanol) and placed in Samdri-790 same giant axons mediate both fast (escape) and slow (fishing) swim- (Tousimis Research Corporation, Rockville, MD) for Critical point dry- ming by utilizing two different spikes, with sodium and calcium ionic ing. After the drying process, the tissues were placed on the holding mechanisms, respectively (Mackie & Meech, 1985, 1995a, 1995b; platforms and processed for metal coating on Sputter Coater (SPI Meech, 2015). Sputter). SEM analyses and photographs were done on the NeoScope Twelve functional neural and two conductive epithelial systems JCM-5000 microscope (JEOL Ltd., Tokyo, Japan). were described in Aglantha, leading to the suggestion that Aglantha possesses a functional analog of the central nervous system, in the form of annulus rather than a compact ganglion (summarized by 2.3 | Immunocytochemistry and phalloidin staining [Mackie, 2004]). Cnidarians independently (from some bilaterians and ctenophores) evolved striated muscles as an additional adaptation to Adult Aglantha were fixed overnight in 4% paraformaldehyde in 0.1 M fast jet-propulsion swimming. phosphate-buffered saline (PBS) at +4–5 C and washed for several In the past, Aglantha has been studied intensively by several hours in PBS. The fixed animals were then dissected into smaller researchers both neurophysiologically and structurally (Arkett, pieces to get better access to specific organs and areas of interest, Mackie, & Meech, 1988; Donaldson, Mackie, & Roberts, 1980; and better antibody penetration. Kerfoot, Mackie, Meech, Roberts, & Singla, 1985; Mackie, 1980, The dissected tissues were preincubated overnight in a blocking 2004; Mackie, Marx, & Meech, 2003; Mackie & Meech, 1985, 1995a, solution of 6% goat serum in PBS and then incubated for 48 hours at 1995b, 2000, 2008; Meech & Mackie, 1993a, 1993b, 1995; Roberts & +4–5 C in the primary antibodies diluted in 6% of the goat serum at Mackie, 1980; Singla, 1978b, 1983; Weber et al., 1982). However, lit- a final dilution 1:50. The rat monoclonal antitubulin antibody (AbD tle is known about the neurotransmitter organization in Aglantha. For Serotec Cat# MCA77G, RRID: AB_325003) recognizes the alpha sub- example, it was reported that nitric oxide signaling controls swimming, unit of α-tubulin, specifically binding tyrosylated α-tubulin possibly via nitrergic sensory neurons in tentacles (Moroz, Meech, (Wehland & Willingham, 1983; Wehland, Willingham, & Sandoval, Sweedler, & Mackie, 2004), and peptidergic innervation of feeding/ 1983). Following a series of PBS washes for 8–12 hr, the tissues were receptive systems was also proposed (Mackie, Singla, & Stell, 1985). incubated for 24 hr in secondary goat anti-rat
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