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Key Aspects of the Iodine Metabolism in Brown Algae: a Brief Critical Review

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Key Aspects of the Iodine Metabolism in Brown Algae: a Brief Critical Review Metallomics KEY ASPECTS OF THE IODINE METABOLISM IN BROWN ALGAE: A BRIEF CRITICAL REVIEW Journal: Metallomics Manuscript ID MT-CRV-11-2018-000327.R1 Article Type: Critical Review Date Submitted by the 04-Feb-2019 Author: Complete List of Authors: Carrano, Carl; San Diego State University, Chemistry and Biochemistry Küpper, Frithjof; University of Aberdeen, Oceanlab Page 1 of 26 Metallomics 1 2 3 4 5 6 KEY ASPECTS OF THE IODINE METABOLISM IN BROWN ALGAE: A 7 BRIEF CRITICAL REVIEW 8 9 10 11 12 13 14 15 16 Frithjof C. Küpper‖†III and Carl J. Carrano†* 17 18 19 20 21 †Department of Chemistry and Biochemistry, 22 San Diego State University 23 San Diego, CA 92182-1030 USA 24 25 26 ‖ School of Biological Sciences, University of Aberdeen, Cruickshank Building, St 27 Machar Drive, 28 Aberdeen AB24 3UU, Scotland, UK 29 30 III 31 Marine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, 32 Aberdeen AB24 3UE, Scotland, UK 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 *Author for correspondence: email [email protected]; phone 619-594-1617; fax 53 54 619-594-4634 55 56 Running Title: Iodine metabolism in Brown Algae 57 58 1 59 60 Metallomics Page 2 of 26 1 2 3 Table of Contents Entry 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 Giant kelp (Macrocystis pyrifera, pictured here: in Port William, East Falkland, Feb. 50 51 2013) has a prolific halogen metabolism. 52 53 (Photo: F.C. Küpper) 54 55 56 57 58 2 59 60 Page 3 of 26 Metallomics 1 2 3 Abstract 4 5 Brown algae include the strongest accumulators of iodine known among living systems. 6 7 This paper reviews the current state of bioinorganic research in the field, focusing on 8 the models Laminaria digitata, Macrocystis pyrifera and Ectocarpus siliculosus, and 9 covering uptake and efflux, localization and biological significance of storage, as well as 10 11 marine and atmospheric chemistry of iodine. 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 3 59 60 Metallomics Page 4 of 26 1 2 3 4 5 6 Significance to Metallomics 7 8 9 10 Although bioinorganic chemistry is often associated with biologically active metals, there 11 12 are other inorganic elements that are important to life. Here we go down one of the less 13 14 traveled paths of bioinorganic chemistry to focus on a halogen, iodine. Iodine has some 15 16 metal-like character and it certainly is inorganic! While its essential role in human 17 18 19 metabolism in the form of the thyroid hormones (such as thyroxine) is well known, fewer 20 21 are aware of its extensive role in the metabolism of brown seaweeds, information of 22 23 which is largely confined to the atmospheric and phycology literature. One of the basic 24 25 26 hypotheses concerning the origins of life is that reactions based on, or catalyzed by, 27 28 simple inorganic elements were likely precursors of the complex organic based 29 30 biological processes characteristic of later life forms. Attack by pathogens and, after the 31 32 33 great oxygenation event, oxidative stress, led to the evolution of forms of innate 34 35 immunity and antioxidant capabilities such as those seen in modern plants and animals. 36 37 It seems possible, if not probable, that these processes may have had a strictly 38 39 inorganic beginning. The brown algae, which constitute a very old lineage, are perhaps 40 41 42 unique in having forms of antioxidants and innate immunity that appear to be strictly 43 44 inorganic and based on iodine. As such, the study of these inorganic based processes 45 46 can possibly shed some light on their evolutionary history. Thus here we review the 47 48 49 fascinating bioinorganic chemistry of iodine in this environmentally important group of 50 51 marine algae. 52 53 54 55 56 57 58 4 59 60 Page 5 of 26 Metallomics 1 2 3 Why Algae? Algae are a polyphyletic assemblage of autotrophic, plant-like organisms, 4 5 6 which generally live in aquatic environments and lack the typical structure (roots-stem- 7 8 leaves) and tissues of terrestrial plants. Marine algae are critically important plant-like 9 10 members of the ocean community which make up most of global marine primary 11 12 productivity and influence climate by controlling processes such as biogenic 13 14 1 15 calcification, oceanic sequestration of CO2 and release of dimethylsulfide . In addition 16 17 many microalgae (phytoplankton), including the climatically important diatoms, 18 19 dinoflagellates and coccolithophores, can form blooms containing toxic or harmful 20 21 22 species that have occurred with increasing frequency in recent decades, and have 23 24 caused substantial ecological and economic damage worldwide. Likewise the 25 26 macroalgae or seaweeds, brown algae in particular, can be the dominant organisms, in 27 28 29 terms of biomass, of the marine coastal environment often forming extensive kelp 30 31 forests. 32 33 34 Brown algae (Phaeophyta) belong to a lineage that has evolved independently of 35 36 other major photosynthetic lineages, such as green plants (Chlorophyta) and red algae 37 38 39 (Rhodophyta). Instead, they are classified within the Stramenopiles and 40 41 Chromalveolates together with diatoms, golden-brown algae and oomycetes 2. They 42 43 also represent one of the few eukaryotic linages that have developed multicellularity. As 44 45 46 a consequence of this singular evolutionary history, brown algae exhibit many unusual, 47 48 and often unique, features. These features are adaptations to the potentially harsh 49 50 marine coastal environments in which brown algae are often the dominant organisms in 51 52 terms of biomass. The key role of kelp forests, effectively constituting an interface 53 54 55 between the ocean, the atmosphere and land masses, in the biogeochemical cycle of 56 57 58 5 59 60 Metallomics Page 6 of 26 1 2 3 halogens is well established 3. Their role in marine benthic carbon sequestration is the 4 5 4 6 subject of ongoing research and there is concern about their regression or changes in 7 8 keystone composition and ecosystem functioning in the context of climate change 5 The 9 10 industrial exploitation of marine algae is also expanding due to interest in their use for 11 12 production of phycocolloids such as agar and carrageenans, alginate, fucans etc., but 13 14 15 also for their potential as biofuels where they have the advantage of high productivity 16 17 without competing with terrestrial crops for farmland. The alginate industry already 18 19 former supports an economic activity of several hundred million dollars annually. Finally 20 21 22 it may be mentioned that many are also of major economic importance as an important 23 24 foodstuff in Asia and particularly in Japan and Korea (nori, kombu, wakame). 25 26 27 While there are many marine macroalgal species that accumulate iodine here we 28 29 focus our attention on three of the most widely studied brown algae that occupy different 30 31 32 ecological niches and compare their iodine metabolism. Ectocarpus siliculosus is a 33 34 filamentous brown alga which has a worldwide distribution along temperate coastlines 35 36 and is a nuisance as a fouling organism on many man-made surfaces in the sea. It has 37 38 39 many significant advantages as an experimental model since it can be readily cultured 40 41 in the laboratory, many facets of its biology have been well studied 6 and it is the only 42 43 brown alga whose genome has been sequenced 7. While Ectocarpus is a small brown 44 45 46 alga with only two cell types, Macrocystis pyrifera (giant kelp) is characterized by large 47 48 size and complex morphology, including meristems that repeatedly split and the 49 50 occurrence of gas-filled pneumatocysts that buoy the thallus at the sea surface and a 51 52 variety of both tissue and cell types (meristoderm, hyphal, cortical, sieve etc.). 53 54 55 Macrocystis dominates the coastal ecosystem from the Pacific coast of central Baja 56 57 58 6 59 60 Page 7 of 26 Metallomics 1 2 3 California, México, to central California, USA, and parts of coastal Alaska. Macrocystis 4 5 6 is also the dominant canopy forming kelp throughout much of the coastal ecosystems in 7 8 the southern Hemisphere 8. Macrocystis is of paramount ecological and economic 9 10 importance as it is the single largest source of raw material for the global alginate 11 12 industry. Finally Laminaria digitata (Oarweed), is the major kelp species on North 13 14 15 Atlantic rocky shores, including Maine and the Canadian Maritimes, Newfoundland and 16 17 the European Atlantic coast from Brittany (France) to northern Norway. It is the 18 19 strongest iodine accumulator among all living systems that is currently known 9, and its 20 21 10-12 22 iodine emissions have an established impact on aerosol formation . 23 24 25 Environmental Aspects: Brown algae are unique in that they feature a highly evolved 26 27 halogen metabolism. The genus Laminaria comprises the strongest accumulators of 28 29 iodine currently known and are major emitters of both molecular iodine and iodinated 30 31 11 32 organics into the atmosphere .
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