Aldehyde-encapsulating liposomes impair marine grazer survivorship

Abstract

SUMMARYIn the last decade, there has been an increased awareness that secondary metabolites produced by marine diatoms negatively impact the reproductive success of their principal predators, the copepods. Several oxylipins, products of the enzymatic oxidation of fatty acids, are produced when these unicellular algae are damaged, as occurs during grazing. In the past, the dinoflagellate Prorocentrum minimum, which does not produce the oxylipin 2-trans,4-trans-decadienal (DD), has been used as a live carrier to calculate daily ingestion rates of this molecule by copepod crustaceans. However, since the interaction between oxylipins and live carriers is unknown, the question as to how much and for how long ingestion of these molecules affects copepod reproduction remains a critical point to understanding the functional role of such compounds at sea. In the investigation presented here we used giant liposomes (~7·m) as a delivery system for the oxylipin DD, prepared in the same size range as copepod food and containing known amounts of DD. The aim of this work was to relate the ingestion of DD to the reproductive failure of the copepods Temora stylifera and Calanus helgolandicus. Liposomes were very stable over time and after 10·days of feeding, liposomes encapsulating DD reduced egg hatching success and female survival with a concomitant appearance of apoptosis in both copepod embryos and female tissues. Concentrations of DD inducing blockage were one order of magnitude lower that those used in classical feeding experiments demonstrating that liposomes are a useful tool to quantitatively analyze the impact of toxins on copepods.

Toxigenic effects of diatoms on grazers, phytoplankton and other microbes: a review

“…Hence, these compounds differ from those that act as feeding deterrents, the purpose of which is not to intoxicate the predator but discourage further consumption, or those that lead to physical incapacitation such as paralysis and death of the predator. Cembella (2003) termed such stealth compounds of low acute toxicity to adult predators that lead to post-digestive reduction in fecundity or depressed viability the ''kill-the-children'' selection, even though recent evidence suggests that these compounds compromise adult fitness as well (Buttino et al 2008). It simply takes longer for these effects to manifest themselves in adults compared to larval stages, as had already been observed by Taylor et al (2007).…”

“…In another study, Buttino et al (2008) used these giant liposomes to encapsulate decadienal in order to investigate the effect of PUAs on the reproductive biology of the copepods Temora stylifera and Calanus helgolandicus. After 10 days of feeding, liposomes reduced egg hatching success and female survival with a concomitant appearance of apoptosis in both copepod embryos and female tissues.…”

Impact of the diatom oxylipin 15S-HEPE on the reproductive success of the copepod Temora stylifera

“…Like PUAs, 15S-HEPE probably accumulates in the gonads the longer the female feeds on diets containing this metabolite. Accumulation of such toxins has been shown by Buttino et al (2008) using decadienalencapsulating giant liposomes supplemented to a diet of P. minimum. After 10 days of feeding, egg hatching success and female survival were dramatically reduced with a concomitant appearance of apoptosis in both copepod embryos and female tissues.…”

Apoptosis to predict copepod mortality: state of the art and future perspectives

“…Therefore, cells undergoing apoptosis appear green in fluorescence. This probe was used to detect apoptotic embryos spawned by the copepod Calanus helgolandicus fed giant liposomes encapsulating known concentrations of a diatom-derived aldehyde (Buttino et al, 2008) (Fig. 2).…”

“…More recently, a link between induction of PCD and environmental stress has been established in many marine organisms (Carnevali et al, 2003;Poulet et al, 2003;Romano et al, 2003;Tosti et al, 2003;Ianora et al, 2004;Migliarini et al, 2005;Buttino et al, 2008). Here, we review recent progress in the study of induction and detection of apoptosis in zooplankton copepods, after their exposure to different apoptoticinducer compounds, and we propose methods to predict copepod mortality even when organisms appear normal.…”