The jellyfish genome sheds light on the early evolution of active predation

Abstract

59Background: Unique among cnidarians, jellyfish have remarkable morphological and 60 biochemical innovations that allow them to actively hunt in the water column. One of the first 61 animals to become free-swimming, jellyfish employ pulsed jet propulsion and venomous 62 tentacles to capture prey. 63Results: To understand these key innovations, we sequenced the genome of the giant Nomura's 64 jellyfish (Nemopilema nomurai), the transcriptomes of its bell and tentacles, and transcriptomes 65 across tissues and developmental stages of the Sanderia malayensis jellyfish. Analyses of 66 Nemopilema and other cnidarian genomes revealed adaptations associated with swimming, 67 marked by codon bias in muscle contraction and expansion of neurotransmitter genes, along with 68 expanded Myosin type II family and venom domains; possibly contributing to jellyfish mobility 69 and active predation. We also identified gene family expansions of Wnt and posterior Hox genes, 70 and discovered the important role of retinoic acid signaling in this ancient lineage of metazoans, 71 which together may be related to the unique jellyfish body plan (medusa formation).72 Conclusions: Taken together, the jellyfish genome and transcriptomes genetically confirm their 73 unique morphological and physiological traits that have combined to make these animals one of 74 the world's earliest and most successful multi-cellular predators. 75 76 Background 80 Cnidarians, including jellyfish and their predominantly sessile relatives the coral, sea anemone, 81 and hydra, first appeared in the Precambrian Era and are now key members of aquatic 82 ecosystems worldwide [1]. Between 500 and 700 million years ago, jellyfish developed novel 83 physiological traits that allowed them to become one of the first free-swimming predators. The 84 life cycle of the jellyfish includes a small polypoid, sessile stage which reproduces asexually to 85 form the mobile medusa form that can reproduce both sexually and asexually [2]. The class 86 Scyphozoa, or true jellyfish, are characterized by a predominant medusa life-stage consisting of a 87 bell and venomous tentacles used for hunting and defense [3]. Jellyfish medusae feature a 88 radially symmetric body structure, powered by readily identifiable cell types such as motor 89neurons and striated muscles that expand and contract to create the most energy-efficient 90 swimming method in the animal kingdom [4, 5]. Over 95% water, jellyfish are osmoconformers 91 that use ion gradients to deliver solutes to cells and tissues where sodium and calcium ions 92 activate the muscle contractions that power their propulsion. Notably, many jellyfish species can 93 survive in habitats with varying levels of salinity and are successful in low-oxygen environments, 94 allowing them to bloom even in dead zones [6]. These innovations have allowed them to 95 colonize aquatic habitats across the globe both in brackish and marine environments, spanning 96 the shallow surface waters to the depths of the seas. 97 98 Results and discussion 99

Insights into the evolution of digestive systems from studies of Trichoplax adhaerens

“…Fluorescence in situ hybridization with probes against Trichoplax trypsin, chymotrypsin, and phospholipase A2 confirmed that spatial distribution of cells expressing these enzymes matches that of lipophil cells labeled with a lipophilic dye (C. Smith and T. Mayorova, unpublished observations). There is experimental evidence that lipophilic granules in Trichoplax contain toxins (Jackson and Buss 2009) and several toxins have been identified in the Trichoplax genome (Jackson and Buss 2009;Kim et al 2018). To our knowledge, lipids have not been detected in digestive granules in animals other than Placozoa.…”