Enzymatic Characterization of the Morphogen Recognized by Agaricia humilis (Scleractinian Coral) Larvae

Abstract

Larvae of the common Caribbean scleractinian coral, Agaricia humilis, are induced to settle and metamorphose by contact with specific crustose (nongeniculate) coralline red algae. This requirement for an exogenous trigger of settlement and metamorphosis has been shown to control the distribution of recruits of this coral in the natural environment. Results reported here demonstrate that the stringency and specificity of this larval requirement persist for at least 30 days following the planktonic release of the brooded larvae, thus enhancing both the capacity for dispersal of the larvae and the substratum specificity of their metamorphosis and recruitment. The inducer of metamorphosis is shown to be associated with an insoluble macromolecular carbohydrate. This molecule is found with the partially purified cell walls obtained from a morphogenetic crustose red alga, Hydrolithon boergesenii, or its associated microflora. Because two non-inductive crustose red algal species also lack the cell wall-associated inducer, the substratum specificity of metamorphosis is probably the result of larval recognition of this molecule. In procedures that should prove widely applicable to other systems, purified and highly specific enzymes were used to cleave the inductive cell wall-associated polysaccharides and to solubilize the active morphogen. Enzymes were also used as probes with which to identify essential structural features required for the morphogenetic activity. These enzymatic and related biochemical studies show that the morphogen is associated with, and may itself contain, a sulfated glycosaminoglycan that includes multiple N-acetylglucosamine and galactose residues. The larval receptors that recognize this complex carbohydrate cue may thus be related to lectins. The solubilized morphogen induces normal settlement, attachment, and the metamorphosis of A. humilis and A. tenuifolia larvae on clean polystyrene surfaces, and the larvae seem to have no other requirement. This effect is apparently specific for larvae of species induced to settle by the intact alga; larvae of the sympatric coral Tubastraea aurea are not induced by this chemical, or by the intact algal surface. A wide variety of other natural and synthetic sulfated polysaccharides and related polymers have little or no inductive effect on the A. humilis larvae, suggesting that the larval receptors involved in substratum recognition are highly specific. A similar high specificity of lectin- and sulfated polysaccharide-mediated recognition, and the resulting control of differentiation, has been observed in a wide variety of biological systems.

Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals

“…Laboratory investigations of larval competency in corals show that the planulae of both spawners and brooders may continue in the planktonic phase for many weeks if no substrate is available (Richmond 1987a, Morse & Morse 1991, Morse et al 1996, Wilson & Harrison 1998. Moreover, the duration of the planktonic phase differs among species, even among those with the same reproductive mode.…”

A proline-rich peptide originating from decomposing mangrove leaves is one natural metamorphic cue of the tropical jellyfish Cassiopea xamachana

“…During the past decade a number of studies have focussed on the identification of natural metamorphic cues in an attempt to test whether models established in the laboratory may work in nature, as well as to explain distribution of individuals in certain specific habitats (e.g. Hadfield & Pennington 1990, Morse & Morse 1991, Tamburri at al. 1992, Leitz & Wagner 1993, Rittschof 1993, Gibson 1995, Forward et al 1996, Lambert et al 1997, Walters et al 1997, Wieczorek & Todd 1997, Avila 1998).…”

“…However, progress has been slow, and to date most cues originating from substrata in the environment have only been partially characterized (e.g. Morse & Morse 1991, Pawlik 1992, Leitz & Wagner 1993, Zimmer-Faust & Tamburri 1994, Lambert et al 1997.…”

Benthic habitat map of U.S. Coral Reef Task Force Faga‘alu Bay priority study area, Tutuila, American Samoa

“…Crustose coralline algae (CCA) can be beneficial as it encrusts and binds reef rubble, thus providing a stable substrate for coral recruitment after a major disturbance. CCA has also been shown to induce metamorphosis and settlement of coral larvae as well as increase survivorship of recruits (Morse and others, 1988;Morse and Morse, 1991;Heyward and Negri, 1999;Raimondi and Morse, 2000;Harrington and others, 2004). Many of the small corals (<100 cm in diameter) found on reef rubble on the reef flat have likely attached or settled since the 2009 tsunami, and their subsequent growth may be indicative of the coral reef ecosystem's slow recovery.…”