Mycosporine-like amino acids are multifunctional molecules in sea hares and their marine community

Abstract

Molecules of keystone significance are relatively rare, yet mediate a variety of interactions between organisms. They influence the distribution and abundance of species, the transfer of energy across multiple trophic levels, and thus they play significant roles in structuring ecosystems. Despite their potential importance in facilitating our understanding of ecological systems, only three molecules thus far have been proposed as molecules of keystone significance: saxitoxin and dimethyl sulfide in marine communities and tetrodotoxin in riparian communities. In the course of studying the neuroecology of chemical defenses, we identified three mycosporine-like amino acids (MAAs)-N-ethanol palythine (= asterina-330), N-isopropanol palythine (= aplysiapalythine A), and N-ethyl palythine (= aplysiapalythine B)-as intraspecific alarm cues for sea hares (Aplysia californica). These alarm cues are released in the ink secretion of sea hares and cause avoidance behaviors in neighboring conspecifics. Further, we show that these three bioactive MAAs, two [aplysiapalythine A (APA) and -B (APB)] being previously unknown molecules, are present in the algal diet of sea hares and are concentrated in their defensive secretion as well as in their skin. MAAs are known to be produced by algae, fungi, and cyanobacteria and are acquired by many aquatic animals through trophic interactions. MAAs are widely used as sunscreens, among other uses, but sea hares modify their function to serve a previously undocumented role, as intraspecific chemical cues. Our findings highlight the multifunctionality of MAAs and their role in ecological connectivity, suggesting that they may function as molecules of keystone significance in marine ecosystems.

The relationship between UV-irradiance, photoprotective compounds and DNA damage in two intertidal invertebrates with contrasting mobility characteristics

“…However, although MAA levels in A. tenebrosa during summer are not maximal, the levels present would still provide some degree of protection against UV-A and, considering both shinorine [72] and porphyra have been shown to have antioxidant capacity [73], potentially UV-A + UV-B induced oxidative stress. Other studies have also demonstrated that MAA levels are often not high enough throughout most of summer to completely protect DNA from UV-B damage [22,71,[74][75][76][77] and the results of these studies are consistent with our observation that CPD levels are approximately twice as high in A. tenebrosa during the summer periods, when animals were exposed to high UV-R doses, than in D. aethiops. Considering the sessile nature of A. tenebrosa, and the lack of any physical adaptations to reduce the impact of UV-R, this sea anemone will most likely require efficient mechanisms to repair DNA damage and keep CPD levels below that which could result in cell death.…”

The sedoheptulose 7-phosphate cyclases and their emerging roles in biology and ecology

“…2, 18, 19, 32 These organisms have a fused divergent DDGS and O-MT, unlike traditional MAA gene clusters where the DDGS and O-MT are discrete. Phylogenetic analysis suggests that multiple horizontal gene transfer (HGT) events spread this fusion protein, with origins in cyanobacteria and dinoflagellates.…”

“…MAAs have features of keystone molecules, due to their presence throughout many trophic levels, yet their function differs not only by organism but also within single organisms. 32 In bacteria, production of MAAs has been associated with providing protection against UV damage, salt stress, and high ammonium due to increased MAA levels under these conditions. 22, 28, 41, 42 In the cyanobacterium Microcystis aeruginosa , shinorine was found in the slime layer, where it appears to have a primary structural role in the sheath and a limited role in UV protection.…”

Ink From Longfin Inshore Squid, Doryteuthis pealeii, as a Chemical and Visual Defense Against Two Predatory Fishes, Summer Flounder, Paralichthys dentatus, and Sea Catfish, Ariopsis felis

“…A third mechanism is sensory inactivation, in which the ink secretion partially blocks the activity of peripheral chemoreceptors of predators and thereby affects the predators' ability to detect and respond to appetitive cues (LoveChezem et al, 2013). The ink of sea hares also contains intraspecific alarm cues that evoke escape behaviors of conspecific sea hares, thus also functioning as an antipredatory chemical defense (Fiorito and Gherardi, 1990;Kicklighter et al, 2007Kicklighter et al, , 2011. The diversity of defensive mechanisms allows sea hares to defend themselves against various species of predators (depending on the predators' sensitivity to the chemicals); against various individuals of a given species of predator (depending on the individual's physiological state, such as hunger); and in different envi-ronments (in the absence of foods containing diet-dependent chemical defenses).…”