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Mesoglea

Mesoglea is the gelatinous extracellular matrix that separates the ectodermal (epidermis) and endodermal (gastrodermis) cell layers in diploblastic animals, including cnidarians such as jellyfish, corals, and sea anemones, as well as ctenophores; it is generally acellular in cnidarians but contains cells such as muscle and nerve cells in ctenophores, serving as a flexible supportive structure essential to their body plan.^[1] Composed primarily of fibrillar collagens, collagen IV, laminin subunits, and proteins like thrombospondin in cnidarians, it forms a sheet-like layer with a basement membrane adjacent to each epithelial layer and a central fibril-rich region, resembling vertebrate connective tissue.^[2] In polyps, the mesoglea is typically thin, contributing to a hydrostatic skeleton that aids attachment and stability, while in medusae, it is thick and jelly-like, providing buoyancy and enabling pulsatile swimming through muscle contractions against water pressure.^[3] The mesoglea plays critical roles beyond mechanical support, including facilitating nutrient diffusion from the gastrovascular cavity in the absence of a circulatory system and limiting body wall thickness to promote gas exchange by diffusion.^[1] In species like the upside-down jellyfish Cassiopea sp., it functions as a physico-chemical buffer, acting as an oxygen reservoir with concentrations up to 500 μmol O₂ l⁻¹ during photosynthesis by symbiotic algae and stabilizing pH fluctuations (from ~8.8 in light to acidic conditions near the surface in darkness), which protects the microenvironment for photosymbionts.^[4] During regeneration, as observed in the sea anemone Anemonia viridis, the mesoglea reorganizes through collagen deposition and remodeling by fibroblast-like cells, forming a scaffold that guides tissue reconstruction and enhances stiffness post-injury.^[5] Additionally, components like thrombospondin in Hydra regulate developmental processes, such as restricting head organizer formation via negative feedback on Wnt/β-catenin signaling.^[2] Though generally acellular in cnidarians, it may contain scattered amoebocytes or other cells in some species, and its composition varies across cnidarian classes, reflecting adaptations to diverse habitats from freshwater to marine environments. In ctenophores, the mesoglea is more cellular and supports different locomotion mechanisms.^[5]^[6]

Introduction

Definition and Basic Characteristics

Mesoglea is defined as the acellular or sparsely cellular gelatinous layer positioned between the ectoderm and endoderm in diploblastic animals, such as cnidarians and ctenophores.^[6] This extracellular matrix serves as a structural intermediary in these radially symmetric organisms, which lack a true mesoderm found in triploblastic bilaterians.^[7] In cnidarians, it forms the bulk of the body in medusae forms like jellyfish, while in ctenophores, it provides a similar supportive role between their epithelial layers.^[8] The basic characteristics of mesoglea include its high water content, typically comprising up to 95-96% water, which contributes to its jelly-like consistency and buoyancy.^[9] The remaining composition consists primarily of proteins such as collagen and other structural proteins, along with polysaccharides and minor amounts of salts, rendering it transparent, flexible, and resilient.^[10] This matrix is often acellular but may contain scattered amoeboid cells or fibers, enabling it to function as a hydrostatic supportive structure without rigid skeletal elements. Mesoglea was first described in the mid-19th century through studies of jellyfish anatomy, where researchers like Thomas Huxley and George James Allman identified it as a distinct non-cellular layer distinguishing diploblastic organization from the mesodermal tissues of more complex animals.^[7] This early recognition highlighted its role as an evolutionary precursor to mesoderm-like tissues, based on histological observations of coelenterates.^[7]

Historical Context

The discovery of the mesoglea occurred in the mid-19th century amid detailed anatomical examinations of jellyfish and polyps, which revealed the diploblastic body plan of cnidarians consisting of an outer ectoderm and inner endoderm separated by a gelatinous middle layer. Researchers such as Thomas Henry Huxley, in his 1849 study of jellyfish, and George James Allman, in his 1853 description of polyps, first documented this layered structure, highlighting the middle layer's role as a supportive substance distinct from the cellular epithelia.^[7] These observations built on earlier 18th-century work on coelenterate anatomy but provided the foundational descriptions that established the mesoglea as a key feature of cnidarian organization.^[7] The term "mesoglea" was coined in the late 19th century, around the 1880s, derived from the Greek words "meso" (middle) and "gleia" (glue), to specifically denote the adhesive, jelly-like middle layer in cnidarians. Its first known use in scientific literature dates to 1886, reflecting the growing interest in invertebrate histology during that era.^[11] Initially, the term was sometimes conflated with "mesenchyme," which had been introduced earlier to describe cellular middle layers in poriferans and cnidarians, leading to terminological ambiguity as both referred to interstitial materials between epithelia.^[12] By the 20th century, refinements in microscopy clarified the mesoglea as a distinct extracellular matrix rather than a true germ layer like mesenchyme or mesoderm, emphasizing its primarily acellular composition with embedded fibers and scattered cells. This distinction resolved earlier confusions, positioning the mesoglea as a non-homologous structure to triploblastic mesoderm and reinforcing the diploblastic classification of cnidarians.^[12] Seminal ultrastructural studies in the late 1960s and 1970s, such as those by Haynes, Burnett, and Davis on Hydra, confirmed the mesoglea's non-cellular nature through electron microscopy, revealing its fibrillar architecture and minimal cellular content, which influenced ongoing debates about diploblasty and the absence of true mesoderm in basal metazoans.^[13] These findings underscored the mesoglea's role as an evolutionary innovation for structural support without forming a developmental germ layer.^[13]

Structure and Composition

Extracellular Matrix Components

The mesoglea is predominantly composed of water, which constitutes approximately 95–99% of its total content, imparting its characteristic jelly-like consistency.^[14] Alongside this high hydration, the primary non-cellular components include glycosaminoglycans such as chondroitin sulfate and heparan sulfate, which contribute to the matrix's structural integrity and hydration.^[15] Collagens, notably types IV and V, form essential fibrous elements, with type IV collagen identified in species like Hydra vulgaris through immunocytochemical and biochemical analyses of isolated mesoglea.^[16] Fibronectin-like proteins are also integral, facilitating molecular interactions within the matrix as confirmed by immunoreactivity studies.^[16] The fiber network within the mesoglea consists of microfibrils and bundled collagen fibrils that confer elasticity and tensile strength.^[17] These structures exhibit varying thicknesses, ranging from nanoscale diameters for fine microfibrils to macroscopic scales up to 12 μm for thicker collagen fibers in hydrozoan jellyfish, as observed via electron microscopy and extraction techniques.^[17]^[18] Biochemically, the mesoglea maintains a hydrated gel state primarily through proteoglycans, including heparan sulfate variants, which bind water and ions to stabilize the matrix.^[16] This composition also provides pH and ion buffering capacity, supporting the extracellular environment's homeostasis.^[15] In species such as the jellyfish Aurelia aurita, the mesoglea comprises the majority of the body volume, featuring collagen with a relatively low degree of cross-linking compared to vertebrate types, which enhances its flexibility.^[18]^[19] Embedded cellular elements interact with this non-cellular matrix to influence its organization.^[5]

Cellular Elements

The mesoglea of cnidarians and ctenophores is characterized by sparse cellular elements embedded within its gelatinous extracellular matrix, distinguishing it from more cellular connective tissues in other animals. These cells, comprising a minor fraction of the mesoglea's volume, play essential roles in matrix maintenance and remodeling through secretion and migration.^[5]^[20] The primary cell types include amoebocytes, which are motile, phagocytic cells capable of wandering through the matrix to engulf debris and pathogens. Fibroblast-like cells, often spindle-shaped with extended pseudopodia, are responsible for producing and secreting structural fibers such as collagen. In certain species, particularly within Anthozoa and Scyphozoa, rare muscle-like cells are embedded directly in the mesoglea, contributing to contractility without epithelial attachment. These cell types are loosely scattered, with amoebocytes and fibroblasts representing the most common forms across taxa.^[21]^[5]^[22]^[23] Cell density in the mesoglea is low, often rendering it practically acellular, with cells occupying scattered positions throughout the layer rather than forming dense aggregates. This sparse distribution allows for the matrix's jelly-like consistency while enabling cell migration for localized maintenance activities. Cells move via amoeboid motion or pseudopodial extension, navigating the hydrated matrix to reach sites of need.^[5]^[20]^[24] Interactions between these cells and the matrix are primarily secretory and organizational. Amoebocytes and fibroblast-like cells produce key extracellular matrix proteins, including collagen types, which they assemble into fibrils and scaffolds. For instance, in the scyphozoan jellyfish Aurelia aurita, mesogleal cells synthesize a 47 kDa protein (pA47) that is secreted via exocytosis and incorporates into non-collagenous fibers, enhancing matrix elasticity. Similarly, fibroblast-like cells in anthozoans such as Anemonia viridis secrete collagen I and facilitate its polymerization into structured fibers, directly influencing matrix integrity. These processes underscore the cells' role in dynamic fiber assembly without dominating the acellular nature of the mesoglea.^[24]^[25]^[5]^[26] Cell composition varies across cnidarian classes, with scyphozoans exhibiting higher cellular density and motility—such as numerous amoeboid mesogleal cells in A. aurita—compared to hydrozoans, where the mesoglea is often thinner and lacks significant embedded cells, relying more on epithelial-derived elements for matrix support. This contrast highlights adaptations to differing body plans and lifestyles.^[27]^[28]

Functions

Hydrostatic Skeleton and Buoyancy

The mesoglea serves as a hydrostatic skeleton in cnidarians, functioning as an incompressible, gel-like layer that maintains body shape against the external pressure of the aquatic environment.^[18] Its viscoelastic properties, characterized by an elastic modulus of approximately 20 Pa at low frequencies, allow it to resist deformation while supporting the thin epithelial layers of ectoderm and endoderm.^[29] This structure enables the organism to withstand hydrostatic forces without rigid support, akin to a fluid-filled balloon where internal pressure balances external loads.^[29] In terms of buoyancy, the mesoglea's exceptionally high water content—often reaching 99% by weight—results in a low overall density that facilitates neutral buoyancy, allowing cnidarians to remain suspended in water without continuous muscular effort.^[30] This property is enhanced by its gel composition, which minimizes sinking or floating tendencies in marine habitats. The material's ability to regulate ion concentrations, such as sulfate, further aids in fine-tuning density for buoyancy control.^[31] Biomechanically, the mesoglea derives tensile strength from embedded collagen and fibrillin fibers, achieving up to 0.17 MPa in tension and 1.43 MPa in compression despite its watery matrix, which resists compressive forces during locomotion.^[32] Its viscosity supports slow, controlled deformation, while elasticity permits energy storage and release; in medusae, ectodermal muscle contractions cause radial expansion of the mesoglea, expelling water for jet propulsion and enabling bell volume changes of up to 50%.^[33] Vertical fibers within the mesoglea provide radial integrity, enhancing pulsatile swimming efficiency by recoiling passively after contraction.^[29]

Role in Regeneration and Repair

In cnidarians, the mesoglea plays a critical role in facilitating tissue regeneration following injury, such as tentacle or body column amputation, by reorganizing its extracellular matrix to support cell proliferation and migration. Post-injury, the mesoglea undergoes dynamic remodeling, where resident cells and infiltrating amoebocytes contribute to the reformation of the matrix, restoring structural integrity and enabling the regrowth of lost tissues.^[5] This process highlights the mesoglea's plasticity, allowing it to serve as a dynamic framework rather than a static barrier during repair.^[34] Key repair mechanisms involve amoebocytes, which migrate into the damaged area and deposit new collagenous and elastic fibers to rebuild the mesogleal matrix. These cells differentiate into fibroblast-like forms that synthesize extracellular components, while the existing mesoglea acts as a scaffold guiding epithelial cell migration and differentiation to close wounds and reconstruct tissues.^[5] Additionally, enzymatic activities, such as gelatinolytic proteases, increase in the mesoglea to degrade and reorganize damaged fibers, enhancing matrix stiffness and promoting efficient healing.^[35] In the sea anemone Anemonia viridis, tentacle amputation triggers rapid mesogleal remodeling, with wound closure occurring within 1 day and noticeable regrowth by 7 days post-amputation, ultimately restoring hydrostatic integrity through collagen I deposition by amoebocytes.^[5] Similarly, in the jellyfish Aurelia aurita, studies demonstrate the plasticity of mesogleal cells during regeneration, where they dedifferentiate and contribute to matrix reformation following arm or tentacle loss, underscoring the mesoglea's role in enabling whole-body repair without requiring extensive cell proliferation in early stages.^[36]^[37]

Other Functions

Beyond mechanical support and repair, the mesoglea facilitates nutrient diffusion from the gastrovascular cavity in the absence of a circulatory system and limits body wall thickness to promote gas exchange by diffusion.^[1] In species like the upside-down jellyfish Cassiopea sp., it acts as a physico-chemical buffer, serving as an oxygen reservoir with concentrations up to 500 μmol O₂ l⁻¹ during photosynthesis by symbiotic algae and stabilizing pH fluctuations (from ~8.8 in light to acidic conditions near the surface in darkness), protecting the microenvironment for photosymbionts.^[4] Additionally, components like thrombospondin in Hydra regulate developmental processes, such as restricting head organizer formation via negative feedback on Wnt/β-catenin signaling.^[2]

Occurrence and Variations

In Cnidarians

Mesoglea is a defining feature of all cnidarians, which are diploblastic organisms characterized by two epithelial layers—the ectoderm and endoderm—separated by this acellular or sparsely cellular gelatinous matrix. As the primary structural component, it provides support and flexibility across diverse cnidarian forms, including jellyfish (medusae), corals, and sea anemones (polyps). In scyphozoan medusae, such as Aurelia aurita, the mesoglea reaches its greatest thickness, comprising up to 95-98% water by volume, which contributes to the organism's overall buoyancy and bell-shaped form.^[38]^[39] Adaptations of the mesoglea vary significantly between polypoid and medusoid life stages to suit their respective lifestyles. In sessile polyps, such as those of sea anemones (Actiniaria) and corals (Scleractinia), the mesoglea is typically thinner and more fibrous, reinforced by collagen fibers that enhance rigidity and facilitate attachment to substrates like rocks or sediments.^[23] This fibrous composition supports the polyp's upright posture and resistance to environmental stresses, such as water currents, while maintaining a compact body plan for benthic existence. In contrast, the mesoglea in free-swimming medusae is voluminous and predominantly gelatinous, forming the bulk of the bell and enabling pulsatile contractions for propulsion through water columns.^[15]^[23] Certain cnidarians exhibit unique mesogleal features tied to ecological interactions, though its role remains predominantly structural. In symbiotic corals, the mesoglea occasionally harbors bacterial symbionts, contributing to the holobiont's metabolic stability without altering the matrix's core supportive function.^[40]^[41] Additionally, in cnidarian tentacles, the mesoglea permits dynamic fluid flow, allowing coordinated extension and retraction during prey capture. A notable variation occurs in hydrozoan medusae, where the mesoglea incorporates contractile elements, such as embedded smooth muscle cells, enabling rapid, jet-like swimming bursts that differ from the slower, more passive pulsations in scyphozoan medusae.^[23]^[17]

In Ctenophores

In ctenophores, the mesoglea forms a gelatinous connective tissue layer situated between the outer ectodermal and inner endodermal cell layers, serving as the primary structural component of the body. Unlike the largely acellular mesoglea in cnidarians, the ctenophore version is notably more cellular, incorporating mesenchymal cells, muscle fibers, and nerve elements that contribute to its mucoid consistency and dynamic functionality.^[6] This cellular composition supports the characteristic biradial symmetry of ctenophores, providing a flexible framework that accommodates the arrangement of eight meridional rows of comb plates—ciliated structures essential for locomotion.^[42] Several adaptations distinguish the mesoglea in ctenophores, particularly in relation to their diverse body forms and lifestyles. It tends to be proportionally thinner relative to overall body size compared to the voluminous mesoglea in many medusoid cnidarians, allowing for greater maneuverability in pelagic environments. High levels of collagen IV within the mesoglea confer exceptional flexibility, enabling species with ribbon-like or flattened bodies, such as those in the order Beroida, to undulate efficiently through water.^[43] Additionally, the mesoglea provides structural support for bioluminescent systems, with photocytes—light-emitting endodermal cells—positioned adjacent to its boundary, facilitating rapid signal propagation during nocturnal displays.^[44] Unique to ctenophores, the mesoglea exhibits greater cellular density than in other diploblasts, including diffuse populations of neuron-like cells and intramesogleal nerve nets that integrate sensory and motor functions across the body.^[8] This innervation contrasts with the sparser cellularity in cnidarian mesoglea and supports coordinated behaviors without a centralized brain. Due to reliance on ciliary propulsion via comb plates for locomotion, ctenophores depend less on the mesoglea as a hydrostatic skeleton for jet-like movement, though it still maintains buoyancy through osmotic adjustments, such as pumping water into the mesoglea via ciliary rosettes in brackish conditions. In the invasive ctenophore Mnemiopsis leidyi, the mesoglea's hyper-osmoconforming properties—maintaining osmolarity only slightly above ambient seawater—enable rapid volume and size adjustments in response to salinity fluctuations, facilitating its spread across diverse estuarine and coastal habitats from the Black Sea to the Baltic.^[45]

Evolutionary and Research Perspectives

Evolutionary Origins

The mesoglea is regarded as a primitive extracellular matrix (ECM) ancestral to all metazoans, emerging as a key innovation that facilitated the transition from unicellular to multicellular organization by providing structural support between epithelial layers.^[46] This acellular layer, composed primarily of collagens and other conserved ECM proteins like laminin and perlecan, is retained in diploblastic phyla such as Cnidaria and Ctenophora, where it forms a prominent, jelly-like barrier between the ectoderm and endoderm.^[46] In contrast, triploblastic bilaterians lack mesoglea, having evolved a more differentiated mesoderm with specialized ECM derivatives for internal tissue support.^[47] Fossil evidence from the Ediacaran biota, dating to approximately 575–541 million years ago, points to mesoglea-like structures in early soft-bodied metazoans, exemplified by rangeomorphs such as Charnia and Rangea.^[48] These organisms possessed a thin-walled, bag-like hydrostatic exoskeleton with a central mesoglea-like layer that biomechanically reinforced the integument, separated an external epidermis from an internalized gastrodermis, and enhanced surface area for extracellular digestion.^[48] Such features suggest mesoglea played a pivotal role in enabling macroscopic multicellularity and osmotrophic feeding strategies in pre-Cambrian animals, potentially linking these fossils to stem-group eumetazoans.^[48] The phylogenetic origins of mesoglea are central to ongoing debates about basal metazoan relationships, particularly the relative positions of Ctenophora and Cnidaria.^[49] Traditional views placed cnidarians as the sister group to bilaterians, with ctenophores nested within Eumetazoa, but post-genomic phylogenies often recover ctenophores as the sister lineage to all other metazoans, supported by analyses of genomes from species like Mnemiopsis leidyi and Pleurobrachia bachei.^[49] The presence of mesoglea in both ctenophores and cnidarians bolsters arguments for a non-bilaterian clade, though a ctenophore-first topology implies either ancestral retention with losses in Porifera and Placozoa or convergent evolution of this ECM, challenging linear models of animal diversification.^[49] Molecular investigations since 2013 underscore that mesogleal collagens, particularly collagen IV, predate bilaterian mesoderm, with up to 20 diverse collagen IV genes identified in ctenophores—far exceeding the six in vertebrates—and homologous forms underlying the mesoglea in cnidarians like Nematostella vectensis.^[50] These findings indicate collagen IV as a primordial ECM component essential for basement membrane formation and epithelial integrity at the dawn of metazoan tissues, suggesting convergent evolution of mesoderm-based support systems in triploblasts from an ancient diploblastic-like ancestor.^[50]

Current Research Topics

Recent studies on the symbiosis between cnidarians and photosymbionts have highlighted the mesoglea's role in regulating the physico-chemical microenvironment, particularly in the upside-down jellyfish Cassiopea sp. Microsensor measurements reveal that the mesoglea maintains elevated oxygen levels (up to ~500 µmol O₂ l⁻¹ at depths of 4 mm during illumination) and buffers pH fluctuations, preventing drops below ambient levels in deeper layers even during dark periods when surface pH can decrease by 0.3–0.5 units.^[51] This buffering effect, observed through fiber-optic and electrochemical sensors in intact medusae, supports photosymbiont productivity by mitigating hypoxia and acidification, potentially enhancing mutualistic nutrient exchange under varying light conditions.^[51] Biotechnological applications of mesoglea-inspired materials leverage its hydrogel-like properties for tissue engineering, with research demonstrating superior mechanical strength and anisotropic swelling compared to synthetic hydrogels of similar water content (>95%).^[52] For instance, jellyfish mesoglea-derived collagen scaffolds promote anti-inflammatory responses in macrophages and angiogenesis, offering sustainable alternatives for wound healing and regenerative scaffolds.^[53] Additionally, investigations into cnidarian regenerative processes, including the role of pluripotent i-cells in Hydractinia symbiolongicarpus and amoebocytes in the mesoglea, reveal potential for stem cell-based therapies, including insights into oncogene regulation that could inform anti-cancer strategies through conserved pathways like NF-κB/STAT.^[54] Environmental research examines the mesoglea's contributions to the success of invasive gelatinous species, such as the ctenophore Mnemiopsis leidyi, whose blooms disrupt ecosystems by altering food webs and reducing fish stocks through zooplankton predation. Blooms persist in invaded regions like the Mediterranean and Baltic Seas despite predation pressures. Climate change exacerbates these dynamics by influencing jellyfish physiology; elevated temperatures enhance metabolic rates and bloom formation, with potential responses to ocean acidification. In the 2020s, advanced imaging techniques have elucidated mesoglea dynamics during regeneration in the sea anemone Anemonia viridis, revealing temporal ECM reorganization post-tentacle amputation. Transmission electron microscopy and immunofluorescence show increased mesoglea stiffness and collagen I scaffold formation by day 7, driven by amoebocyte differentiation into fibroblast-like cells.^[26] Positron emission tomography tracks endosymbiont migration and tissue repair up to day 14, while gene expression analyses indicate upregulated Col24a1 (collagen type XXIV alpha 1) at early stages (6 hours post-injury) for mesoglea remodeling, with altered patterns under thermal stress simulating climate scenarios.^[55]^[56] These findings underscore mesoglea's active role in regenerative gene networks, providing models for stress resilience.^[56]

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