The influence of bioactive oxylipins from marine diatoms on invertebrate reproduction and development

Abstract

Diatoms are one of the main primary producers in aquatic ecosystems and occupy a vital link in the transfer of photosynthetically-fixed carbon through aquatic food webs. Diatoms produce an array of biologically-active metabolites, many of which have been attributed as a form of chemical defence and may offer potential as candidate marine drugs. Of considerable interest are molecules belonging to the oxylipin family which are broadly disruptive to reproductive and developmental processes. The range of reproductive impacts includes; oocyte maturation; sperm motility; fertilization; embryogenesis and larval competence. Much of the observed bioactivity may be ascribed to disruption of intracellular calcium signalling, induction of cytoskeletal instability and promotion of apoptotic pathways. From an ecological perspective, the primary interest in diatom-oxylipins is in relation to the potential impact on energy flow in planktonic systems whereby the reproductive success of copepods (the main grazers of diatoms) is compromised. Much data exists providing evidence for and against diatom reproductive effects; however detailed knowledge of the physiological and molecular processes involved remains poor. This paper provides a review of the current state of knowledge of the mechanistic impacts of diatom-oxylipins on marine invertebrate reproduction and development.

Keywords: apoptosis; developmental stability; polyunsaturated aldehydes; reproductive toxicity; teratogen.

Figure 1

Chemical structures of selected diatom-derived molecules with bioactivities associated with cellular apoptosis and disruption of invertebrate reproductive processes. Structures redrawn from [27,28,30,88].

Figure 2

The percentage of morphologically normal oocytes of Asterias rubens (a) following in vitro exposure to 1.5 μg mL⁻¹ decadienal at either the prophase or metaphase cell cycle stages and (b) exposed during meiotic-reinitiation to either filtered seawater (FSW), cis-5,8,11,14,17-eicosapentaenoic acid (EPA), the saturated-aldehydes decanal and undecanal or the PUA decadienal (DD) at concentrations of 0.5, 1 or 1.5 μg mL⁻¹. Mean (±S.D.) of 3 replicates. Details of experimental design can be found in Caldwell [103].

Figure 3

Asterias rubens oocytes exposed to decadienal at a concentration of 1.5 μg mL⁻¹ (a) control prophase oocyte displaying intact germinal vesicle, (b) control metaphase oocyte having undergone germinal vesicle breakdown, (c&d) oocytes exposed to decadienal at a concentration of 1.5 μg mL⁻¹. 1 = morphologically normal oocyte, 2 = necrotic oocyte. Scale bar = 100 μm. Details of experimental design can be found in Caldwell [103].

Figure 4

The effect of increasing concentration of decadienal on Asterias rubens sperm-front migration velocities. Mean value of three replicate experiments for each concentration ± S.D. Details of the experimental design can be found in Caldwell [103] and Caldwell et al. [72].

Figure 5

Screen grabs of Nereis virens sperm subjected to computer-assisted analysis under exposure to (a) filtered seawater control and (b) 5 μM decadienal [184].

Figure 6

Stagegate model for an embryo affected by pro-apoptotic diatom compounds during development. The initial checkpoint is whether the cell is competent to undergo meiotic-reinitiation. The consequence of failure is oocyte apoptosis, which for many species would then trigger reabsorption of the oocyte nutrients by the mother. Genetic surveillance activated at the midblastula transition may trigger abortion or arrested development. Surviving larvae may then undertake a programme of ‘selective’ apoptosis to eliminate non-viable cells - the extent of such will determine whether the larva is competent for further development. See [5,98,135,142] for examples of each checkpoint.

Figure 7

Induction of morphological abnormalities in 9 day old larvae of Nereis virens due to exposure to decadienal at concentrations of (a) 0, (b) 0.01 and (c) 0.05 μg mL⁻¹ during embryogenesis. Details of experimental design can be found in Caldwell [103].

Figure 8

Simplified life cycle of a hypothetical marine invertebrate indicating the potential stages that diatom-oxylipins could interfere with normal ontogenetic processes. For examples refer to [69,71,72,74,92,98,163].