Research

Cnidaria, which is considered a sister group to the Bilateria, is one of the most ancient multicellular phyla, having evolved 700 million ago. The free-living cnidarians such as jellyfish, sea anemones, corals and hydra are commonly characterized by a single body axis, only two germ layers, namely ectoderm and endoderm, and unique and highly complex stinging capsules. In addition to their morphological simplicity, cnidarians display a high level of developmental plasticity that equips them for shape transformation, regeneration and asexual proliferation during their life cycle. Cnidarians are also key players in the marine ecosystem, acting as reef structure builders and as both predators and prey. Recently, a large group of endoparasites, known as Myxozoa, has been added to this colorful phylum. The myxozoans are morphologically and genetically simple, having lost true gametes, embryogenesis, epithelial structures and a nervous system. However, they have kept the characteristic stinging cells of the phylum.

The unique characteristics of cnidarians, together with their basal position in the evolutionary tree, make this phylum an important group for studies of basic developmental and evolutionary processes, as well as of environmental adaptations. We are interested in understanding cnidarian developmental biology and molecular ecology, as detailed below.

Myxozoa infection pathway

Myxozoa is a large group of obligate parasites that have complex life cycles, infecting both vertebrates (mostly fish) and invertebrates (mostly worms) in freshwater and marine environments worldwide. Myxozoan parasites affect the health of both farmed and wild fish populations, causing disease and mortality. To understand the infection process, we have established a collaboration with Prof. Jerri Bartholomew and Dr. Stephen Atkinson from Oregon State University. Recently, we identified the myxozoan Myxobolus bejeranoi as the mortality-causing agent in aquacultured tilapia in Israel. Tilapia is among the most widely produced and traded food fish in the world and in Israel, it is the main farmed fish. To understand the molecular cascades that are activated during the initial stages of the myxozoan infection process, we combine genomics, transcriptomics and proteomics. We expect that the study will highlight the very early stages of infection, before parasite proliferation, and will reveal how the parasite’s molecular mechanisms successfully avoid the fish immune system. We have just started the project and students who are interested in field and lab work as well as molecular biology and bioinformatics are welcomed to join us.

See link to see myxozoan activation https://youtu.be/VG_r2KQgljQ

Myxozoa life cycle

Myxozoa two type of spores

Developmental programming

Cnidarians undergo a well-defined embryogenic program, but are also capable of propagating by asexual reproduction via fission, budding or strobilation. The ability of cnidarians to activate multiple developmental programs can have profound ecological and evolutionary consequences. Our goal is to understand the critical decision junctions that give rise to developmental programming during cnidarian life cycle. To explore the various stages of sexual and asexual reproduction we are using the sea anemone Nematostella vectensis and the jellyfish Aurelia aurita as model organisms.

Oogenesis : To gain insight into the process of oogenesis, we conducted proteomic analysis at five different stages of this process, from its onset to the first embryonic divisions. Additionally, we compared the proteomic profiles of mature ovulated oocyte of Nematostella to MII oocyte stage of mouse, two organisms that diverged 500 million years ago. Our findings suggest that oocyte proteome template predates the divergence of the cnidarian and bilaterian lineages. Currently, we are testing the role of selected pathways by analyzing protein expression and function. In addition, we are analyzing anemone RNA profiles at different time points during the induction process to reveal the receptors and signaling pathways that lead to oogenesis and support oocyte maturation.

Nematostella during spawning. Picture by Shani Levy

Planula-to-polyp transformation and neurogenesis

GABAB receptor-mediated signaling plays central roles in neuronal differentiation and proliferation in the mammalian brain. We found that GABABR signaling controls such neurogenic functions in the basal sea anemone Nematostella vectensis. Our results show that activation of GABABR signaling using the GABAB agonist baclofen reversibly arrests the critical metamorphosis transition from the planktonic planulae to the sessile polyp life stage, as well as the cnidarian neurogenic program. Using transcriptomic analysis combined with spatial analysis of GABAB baclofen-treated planulae, we revealed that baclofen

downregulated proneural factors. Our results suggest an evolutionarily conserved function for GABABR in regulation of neurogenesis. Currently, we are trying to analyze the signal transduction pathways that lead to neurogenesis arrest.

Jellyfish strobilation

In the class Scyphozoa, where the medusa phase is the dominant part of the life cycle, the polyp’s asexual proliferation results in the production of dozens of juvenile medusas (ephyra) in a repeated segmentation process called strobilation. This rapid proliferation leads to jellyfish outbreaks around the globe, which in the last decade seem to have become more severe and frequent. To study the strobilation process, we use the moon jellyfish Aurelia aurita as a model system. We have generated a large dataset using next-generation sequencing of six developmental stages in order to study strobila and ephyra development. Elucidating the mechanistic processes that give rise to medusa development is essential to our understanding of both jellyfish evolution and proliferation.

Jellyfish bloom

Our recent research uses an interdisciplinary approach to elucidate the physical and biological processes controlling the emergence, dynamics and decline of swarms of Rhopilema nomadica, the most abundant jellyfish along the Israeli coast. We are using multi-platform data to understand the dynamics of individual jellyfish swarms by integrating data from airplanes and drones as well as underwater observations using divers and ROVs. Additionally, we are tagging jellyfish with GPS and compare their movements to those of Lagrangian drifters. To understand the role of bacterial pathogens in the demise of the bloom, we are characterizing the jellyfish microbiome during bloom initiation and decline, using the 16S ribosomal DNA gene as a marker. This is an ongoing study that is co-led by Drs. Daniel Sher and Yoav Lehahn from the Leon H. Charney School of Marine Sciences.

Noga searching for jellyfish

Cnidarian stinging capsules

The Cnidarians' stinging cells manufacture intracellular structures known as cnidocysts, which are cyst capsules loaded with an array of toxins. Upon activation of the capsule, a high internal pressure of 150 bars develops, resulting in the discharge of a folded tubule at an acceleration of 5 x10 6 g immediately releasing the toxin arsenal into the target cell. About 30 subtypes of capsules are known, all function by the same principles but differ in size, shape and tubule length. How is the rigid capsule assembled within the stinging cell? What are the active biological compounds that are delivered into the prey? Can we gain insight into the constraints that shape the capsule?

To answer these questions, we have adopted a multidisciplinary approach that combines biology, fish parasitology, micro- and nanofluidics and drug delivery. We study a group of parasites known as Myxozoa, which has recently been placed within the Cnidaria phylum, in order to decipher stinging cell evolution, development and function. This basic research has important application as these parasites have devastating effects on aquaculture and natural fish populations. To test the physical characteristics and the internal osmotic pressures of the stinging capsules, we utilize fabricated chips and a high-speed camera. To uncover the contents of the stinging capsules, we apply proteomics combined with transcriptomics. Combining molecular data with the physical approach accelerates our understanding of the evolution and function of the stinging capsules.

ביולוגיה התפתחותית ואקולוגיה מולקולרית של צורבים

מערכת הצורבים כוללת את שושנות הים, האלמוגים, ההידרות, המדוזות ויש לה תפקיד חשוב במערך האקולוגי הימי. בנוסף לחקר הצורבים יש השלכות אקולוגיות, אבולוציוניות, רפואיות וכלכליות. בעשור באחרון, יחד עם התפתחות הכלים המולקולרים והריצוף הגנומי צורפה למערכה של הצורבים קבוצה גדולה של טפילים בשם מיקסוזואה, המציגה את המערכה באור חדש ונותנת לנו הצצה לתהליכי התפתחות של מנגנוני הצריבה היחודיים למערכה.

תחומי המחקר העיקריים במעבדה כוללים:

חקר תהליכי התפתחות של מינים כמו מדוזה ושושנת ים שהופיעו לראשונה בשחר האבולוציה, לפני קרוב ל-700 מיליון שנה, והשוואתם עם תהליכי התפתחות בבע"ח מפותחים יותר. המעבדה מתמקדת בשאלות כמו: האם תהליכי הבקרה בהתפתחות הביצית בצורבים משותפים גם להתפתחות הביצית ביונקים? כיצד מתרחש תהליך המטמורפוזה מפגית (לרווה) השוחה בים לפוליפ הצמוד למצע ? או כיצד מפוליפ אחד נוצרות עשרות מדוזות?
חקר מנגנון ההדבקה של המיקסוזואה, טפיל הגורם לתמותה של אמנונים בישראל ולפגיעה קשה בדגי סלמון ואחרים בעולם.
הבנת התהליכים הפיזיקליים והביולוגים המבקרים את פריחת המדוזות.
מחקר של מערכות הזרקה טבעיות בגודל מיקרוסקופי. למנגנון הצריבה של הצורבים יכולת הזרקת נוזלים בלחץ של 150 אטמוספרות בחלקיקי שנייה. במעבדה מתבצע מחקר ביולוגי והנדסי להבנת תהליכי בנית המזרק ויצירת הלחץ במערכת, לצד הבנת הזרימה דרך צינור (מחט) בקוטר ננומטרי.

למעבדה גישה לים התיכון לצד יכולת גידול של שלבי החיים השונים של המדוזות ושושנות הים. המחקר מתמקד בשאלות הנ"ל מרמת בעה"ח השלם דרך המערכת התאית ועד לרמה המולקולרית של ה- RNA והחלבון.

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