Metabolomic Assessment of Induced and Activated Chemical Defence in the Invasive Red Alga Gracilaria vermiculophylla

Abstract

In comparison with terrestrial plants the mechanistic knowledge of chemical defences is poor for marine macroalgae. This restricts our understanding in the chemically mediated interactions that take place between algae and other organisms. Technical advances such as metabolomics, however, enable new approaches towards the characterisation of the chemically mediated interactions of organisms with their environment. We address defence responses in the red alga Gracilaria vermiculophylla using mass spectrometry based metabolomics in combination with bioassays. Being invasive in the north Atlantic this alga is likely to possess chemical defences according to the prediction that well-defended exotics are most likely to become successful invaders in systems dominated by generalist grazers, such as marine macroalgal communities. We investigated the effect of intense herbivore feeding and simulated herbivory by mechanical wounding of the algae. Both processes led to similar changes in the metabolic profile. Feeding experiments with the generalist isopod grazer Idotea baltica showed that mechanical wounding caused a significant increase in grazer resistance. Structure elucidation of the metabolites of which some were up-regulated more than 100 times in the wounded tissue, revealed known and novel eicosanoids as major components. Among these were prostaglandins, hydroxylated fatty acids and arachidonic acid derived conjugated lactones. Bioassays with pure metabolites showed that these eicosanoids are part of the innate defence system of macroalgae, similarly to animal systems. In accordance with an induced defence mechanism application of extracts from wounded tissue caused a significant increase in grazer resistance and the up-regulation of other pathways than in the activated defence. Thus, this study suggests that G. vermiculophylla chemically deters herbivory by two lines of defence, a rapid wound-activated process followed by a slower inducible defence. By unravelling involved pathways using metabolomics this work contributes significantly to the understanding of activated and inducible defences for marine macroalgae.

Engineering or food? mechanisms of facilitation by a habitat‐forming invasive seaweed

“…Native habitat-forming seaweed and seagrass reduce predation by fish on herbivorous amphipods, particularly mobile species like Gammarus, which are at a higher risk of predation than more sedentary nestbuilding species (Van Dolah 1978, Stoner 1982, Duffy and Hay 1994. Moreover, Gracilaria's chemical defenses (Nylund et al 2011) may deter omnivorous predators such as fish and reduce predation on amphipods in Gracilaria (Duffy and Hay 1994). In fact, lower predation rates on epifauna within the structure of chemically defended invasive seaweed are known across multiple taxa, including bivalve recruits and herbivorous isopods Wright 2006, Enge et al 2013).…”

“…Consistent with this, our isotope data show that natural populations of Gammarus consume little Gracilaria, but instead favor a combination of Spartina detritus, microalgae, or periphyton on the sediment surface or on Gracilaria. The low feeding of Gammarus on Gracilaria could reflect the alga's chemical defenses (Nylund et al 2011). Our survivorship experiment showed that a diet comprised of either Spartina detritus or sediment alone increased survivorship relative to Gracilaria.…”

Invasion success of the seaweed Gracilaria vermiculophylla correlates with low palatibility

“…G. vermiculophylla is able to defend itself from feeding by up-regulation of chemical compounds. After wounding, the alga produces -among other substances -arachidonic acid derivates, which were found to deter mesograzers such as the omnivorous isopod Idotea baltica (Nylund et al 2011) or the herbivorous sea snail Echinolittorina peruviana (Rempt et al 2012). It seems likely that these or other substances also act as feeding deterrents against L. brevicula and L. littorea.…”

“…Also, Gracilaria vermiculophylla is capable of defending itself from herbivory by mesograzers: if tissue is damaged -either by artificial mechanical wounding or by grazing -the alga produces oxylipins (Nylund et al 2011, Rempt et al 2012). These compounds deter potential grazers of G. vermiculophylla, such as the omnivorous isopod Idotea balthica (Nylund et al 2011) or the herbivorous sea snail Echinolittorina peruviana (Rempt et al 2012). Wound-activated oxylipins are also molecular messengers that mediate induced defenses of gracilarioids (Wein berger et al 2011).…”

Gracilaria vermiculophylla in the Virginia Coastal Bays: Documenting the Distributionand Effects of a Non-Native Species

“…vermiculophylla tissue (Nylund et al 2011;Rempt et al 2012) make the macroalga unpalatable to herbivores who often choose to consume native macroalgae (Thomsen & McGlathery 2007;Nejrup & Pedersen 2010;Jensen et al 2011;.…”