Domoic acid: The synergy of iron, copper, and the toxicity of diatoms

Abstract

Diatom blooms generated by the alleviation of iron limitation in high nitrate-low chlorophyll (HNLC) regions of the oceans often are composed of pennate diatoms of the genus Pseudo-nitzschia, many of which periodically produce the potent neurotoxin domoic acid. We show that toxigenic diatoms have an inducible high-affinity iron uptake capability that enables them to grow efficiently on iron complexed by strong organic ligands in seawater. This low-iron adaptive strategy requires copper and domoic acid, a copper chelator whose production increases sharply when both iron and copper are limiting. Addition of either domoic acid or copper to seawater improves the growth of Pseudo-nitzschia spp. on strongly complexed iron during deck incubation experiments with natural phytoplankton. Our findings indicate that domoic acid is a functional component of the unusual high-affinity iron acquisition system of these organisms. This system may help explain why Pseudo-nitzschia spp. are persistent seed populations in oceanic HNLC regions, as well as in some neritic regions. Our findings also indicate that in the absence of an adequate copper supply, iron-limited natural populations of Pseudo-nitzschia will become increasingly toxic.

Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health

“…The physiological role of DA was further documented in Maldonado et al (2002) and Wells et al (2005). Maldonado et al (2002) reported that DA production was inversely related to cellular growth rates when cells were limited by low iron or copper availabilities.…”

“…Bates et al, 1989;Martin et al, 1990;Fryxell et al, 1997;Gallacher et al, 2001). It is known that DA leaks, or is actively transported, out of the cells, resulting in high levels of the toxin in the surrounding medium (reviewed by Bates, 1998;Wells et al, 2005). It is therefore reasonable to speculate that this toxin could have an allelopathic effect.…”

“…Additional events consistent with DA toxicity have been identified. In 2002, 87 sea lions were found stranded on beaches from the border of the USA to Ensenada, on the Baja peninsula, and it was assumed that DA toxicity was the cause of this event (Herná ndez-Becerril et al, 2007 (Rhodes et al, 1998), Monterey Bay, California, USA (Wells et al, 2005) and Chesapeake Bay, Maryland, USA (Thessen et al, 2009) . No adverse biological effects were detected.…”

Iron biogeochemistry across marine systems – progress from the past decade

“…Iron colimitations and interactions with other nutrients and trace metals have been observed (e.g. Schulz et al, 2004;Mills et al, 2004;Wu et al, 2003;Wells et al, 2005) and apparently the composition of trace metals and macro nutrients greatly affect natural Fe fertilization efficiency (see Sect. 2.2).…”

“…Once overlooked and neglected (Wells, 1998), progress has been made in understanding the nature and importance of organic colloidal material in seawater and coastal systems and challenged the simple discrimination into particulate and dissolved iron (0.45 or 0.2 µm filtered). Furthermore, dynamic exchange between larger iron particles, colloidal iron, and soluble iron (defined as passing either a 0.02 µm or a 1 kDa filter) also directs interest towards the particulate and soluble phase.…”