The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance

Abstract

Brown algae represent a major component of littoral and sublittoral zones in temperate and subtropical ecosystems. An essential adaptive feature of this independent eukaryotic lineage is the ability to couple oxidative reactions resulting from exposure to sunlight and air with the halogenations of various substrates, thereby addressing various biotic and abiotic stresses i.e., defense against predators, tissue repair, holdfast adhesion, and protection against reactive species generated by oxidative processes. Whereas marine organisms mainly make use of bromine to increase the biological activity of secondary metabolites, some orders of brown algae such as Laminariales have also developed a striking capability to accumulate and to use iodine in physiological adaptations to stress. We review selected aspects of the halogenated metabolism of macrophytic brown algae in the light of the most recent results, which point toward novel functions for iodide accumulation in kelps and the importance of bromination in cell wall modifications and adhesion properties of brown algal propagules. The importance of halogen speciation processes ranges from microbiology to biogeochemistry, through enzymology, cellular biology and ecotoxicology.

Keywords: biogeochemistry; brown algae; defense metabolites; halogen speciation; haloperoxidases.

Figure 1

Methyltransferases mediate the transfer of a methyl group (Me) from SAM to a halide (X: halide ion). After [14].

Figure 2

The most common halogenated alkanes found in effluxes from brown algae. (a) monosubstituted haloalkanes generated by action of SAM transferase; (b) and (c) polysubstituted alkanes supposedly generated as secondary products of V-BrPO action on enols. (see text).

Figure 3

Mono- and diiodotyrosine are found in Laminariales, precursors to thyroxin (found as a thyroid hormone in some invertebrates and in higher animals).

Figure 4

Halogenated phenolic monomers found in brown algae.

Figure 5

Halogenated phenolics from brown algae. (a)-Halogenated fucols found in the Laminariale Analipus japonicus (after [33]) and in the Sargassacea Carpophyllum angustifolium (after [32]). Spheres represent acetylation performed for spectroscopic analysis, or hydroxylation for native molecule. (b)-Halogenated phlorethols found in the Sargassacea Cystophora reflexa (after [29] (see also [32], and in Laminaria ochroleuca (after [31]). (c)-Halogenated fucophlorethols found in the Sargassacea Cystophora reflexa (after [29]). (d)-Non-typical halogenated phenolics from brown algae (after [34] and [25]).

Figure 5

Halogenated phenolics from brown algae. (a)-Halogenated fucols found in the Laminariale Analipus japonicus (after [33]) and in the Sargassacea Carpophyllum angustifolium (after [32]). Spheres represent acetylation performed for spectroscopic analysis, or hydroxylation for native molecule. (b)-Halogenated phlorethols found in the Sargassacea Cystophora reflexa (after [29] (see also [32], and in Laminaria ochroleuca (after [31]). (c)-Halogenated fucophlorethols found in the Sargassacea Cystophora reflexa (after [29]). (d)-Non-typical halogenated phenolics from brown algae (after [34] and [25]).

Figure 6

Halogenated eicosanoids (C18 oxylipins derived from stearidonic acid), isolated from the Laminariale Egregia menziesii [41]. (a) Egregiachloride A and B from stearidonic acic catalysis by 13LOX, cyclopentyl cyclization and subsequent carbocation attack at C16 by chlorine anion. (b) Egregiachloride C, similarly synthesized from eicosapentaenoic acid.

Figure 7

Halogenated eicosanoids (C18 oxylipins derived from stearidonic acid), isolated from the Laminariale Eisenia bicyclis [42].

Figure 8

Halogenated linear nor-sesquiterpenes isolated from Padina tetrastromatica [45], and iodinated meroterpene isolated from Ascophyllum nodosum [46].

Figure 9

Halogen chemistry in Laminaria digitata. The different roles of V-HPO enzymes in brown kelp biology are conveniently contrasted in this diagram of a young whole thallus. In growing tissues of the blade (top), active uptake of iodine prevails as V-IPOs are upregulated to replenish iodine stocks to quench excess hydrogen peroxide (among other functions; see text). Iodine imaging revealed extracellular stocks associated with charged polymers for rapid bioavailability, rather than only intracellular I₂stocks via HOI trans-membrane intake as hitherto believed. In the stipe (middle), mechanical resilience is maintained by outer cuticle hardening coinciding with the highest concentration of immobilized iodine. Metabolite translocation occurs in the softer inner matrix as well as signal molecules of suspected systemy. In the holdfast (bottom), soluble phlorotannins (PP) generated in the Golgi apparatus are contained in cytoplasmic physodes, which burst out in the apoplastic space. Bioadhesion is mediated by V-BrPOs, which cross-link the released PP in the presence of hydrogen peroxide and halide ions. The adhesive is thought to result from macromolecular scaffolds between the oxidized polymers and cell wall alginates.

Figure 10

Iodine biogeochemistry at the Marine Boundary Layer. Schematic view of the link between kelp iodine species emissions and tropospheric iodine photooxidation, based upon current algal physiology, seaweed iodine speciation [71] and atmospheric chemistry [96] knowledge. The photograph features a kelp bed during a spring low tide in the vicinity of Roscoff. The large white arrow represents the contribution of kelps such as Laminaria digitata to the release of molecular iodine (I ₂) directly from its apoplastic and peripheral storage in the form of reduced iodide (I⁻). This oxidation is either catalyzed by endogenous specific vanadium iodoperoxidases (V-IPOs) using photosynthesis or stress- generated hydrogen peroxide (H₂O₂), or exogenously by the strong oxidant O₃, when algae are exposed to air at low tide. These oxidative processes also lead to production of volatile halogenated organic compounds (VHOCs) by kelps (thin white arrow), although an estimated 300-fold lower than I₂ fluxes [88]. Phytoplankton mainly contribute to I cycling through VHOC emission (black arrow above the sea). In the troposphere, atomic iodine (I) released by photolysis from I₂ and photolabile VHOCs, reacts with available O₃ to yield IO, rapidly establishing a photostationary state and consuming O₃ whenever IO reacts either with itself (yielding OIO), HO₂ (yielding HOI) or NO₂ (yielding IONO₂): rather than being re-photolysed to release I atoms. HOI and IONO₂ may be taken up by aerosol particles, releasing the dihalogen species IBr, ICl or I₂ via aqueous reaction with available Br⁻, Cl⁻ or I⁻, respectively, in the presence of sufficient acidity (H⁺). Iodine cycling is also linked to Br and Cl cycling, which speciate through similar chemical reactions in the gas phase leading to similar exchanges with marine aerosols.