Abstract
Volatile halocarbons can deplete the protective stratospheric ozone layer contributing to global climate change and may even affect local climate through aerosol production. These compounds are produced through anthropogenic and biogenic processes. Biogenic halocarbons may be produced as defence compounds, anti-oxidants or by-products of metabolic processes. These compounds include very short-lived halocarbons (VSLH), e.g. bromoform (CHBr3), dibromomethane (CH2Br2), methyl iodide (CH3I), diiodomethane (CH2I2). Efforts to quantify the biogenic sources of these compounds, especially those of marine origin, e.g. seaweeds, phytoplankton and seagrass meadows, are often complicated by inherent biological variability as well as spatial and temporal changes in emissions. The contribution of the coastal region and the oceans to the stratospheric load of halocarbons has been widely debated. This highlights the need to understand the factors affecting the release of these compounds from marine sources for which data for modelling purposes are generally lacking. Seaweeds are important sources of biogenic halocarbons subjected to changing environmental conditions. Huge uncertainties in the prediction of current and future global halocarbon pool exist due to the lack of spatial and temporal data input from coastal and oceanic sources. Therefore, investigating the effect of changing environmental conditions on the emission of VSLH by the seaweeds could help towards better estimations of halocarbon emissions. This is especially important in light of global changes in both climate and the environment, the expansion of seaweed cultivation industry and the interactions between halocarbon emission and their environment. In this paper, we review current knowledge of seaweed halocarbon emissions, how environmental factors affect these emissions and identify gaps in understanding. Our aim is to direct much needed research to improve understanding of the contribution of marine biogenic sources of halocarbons and their impact on the environment.
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Abrahamsson K, Choo KS, Pedersen M, Johansson G, Snoeijs P (2003) Effects of temperature on the production of hydrogen peroxide and volatile halocarbons by brackish water algae. Phytochemistry 6:725–734
Almeida M, Filipe S, Humanes M, Maia MF, Melo R, Severino N, da Silva JA, Frausto da Silva JJ, Wever R (2001) Vanadium haloperoxidases from brown algae of the Laminariaceae family. Phytochemistry 57:633–642
Amachi S, Kamagata Y, Kanagawa T, Muramatsu Y (2006) Bacteria mediate methylation of iodine in marine and terrestrial environments. Appl Environ Microbiol 67:2718–2722
Baden DG, Corbett MD (1980) Bromoperoxidases from Penicillus capitatus, Penicillus lamourouxii and Rhipocephalus phoenix. Biochem J 187:205–211
Baker JM, Sturges WT, Sugier J, Sunnenberg G, Lovett AA, Reeves CE, Nightingale PD, Penkett SA (2001) Emissions of CH3Br, organochlorines, and organoiodines from temperate macroalgae. Chemosphere 3:93–106
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Org J 5:9–19
Bischof K, Hanelt D, Tüg H, Karsten U, Brouwer PEM, Wiencke C (1998) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395
Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Env Sci Bio/Technol 5:141–166
Björn LO, Callaghan TV, Gehrke C, Johanson U, Sonesson M (1999) Ozone depletion, ultraviolet radiation and plant life. Chemosphere Global Change Sci 1:449–454
Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso JP, Havenhand J, Hutchins DA, Riebesell U, Rintoul MS, Vichi M (2018) Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—a review. Glob Chang Biol 24:2239–2261
Bravo-Linares CM, Mudge SM, Loyola-Sepulveda RH (2010) Production of volatile organic compounds (VOCs) by temperate macroalgae. The use of solid phase microextraction (SPME) coupled to GC-MS as method of analysis. J Chil Chem Soc 55:227–332
Brodie J, Williamson CJ, Smale DA, Kamenos NA, Mieszkowska N, Santos R, Cunliffe M, Steinke M, Yesson C, Anderson KM, Asnaghi V, Brownlee C, Burdett H, Burrows MT, Collins S, Donohue PJC, Harvey B, Foggo A, Noisette F, Nunes J, Ragazzola F, Raven JA, Schmidt DN, Suggett D, Teichberg M, Hall-Spencer JM (2014) The future of the Northeast Atlantic benthic flora in a high CO2 world. Ecol Evol 4:2787–2798
Carpenter LJ, Liss PS (2000) On temperate sources of bromoform and other reactive organic bromine gases. J Geophys Res: Atmospheres 105 (D16):20539–20547
Carpenter LJ, Malin G, Liss PS, Küpper FC (2000) Novel biogenic iodine-containing trihalomethanes and other short-lived halocarbons in the coastal East Atlantic. Glob Biogeochem Cycles 14:1191–1204
Carpenter LJ, Jones CE, Dunk RM, Hornsby KE, Woeltjen J (2009) Air-sea fluxes of biogenic bromine from the tropical and North Atlantic Ocean. Atmos Chem Phys 9:1805–1816
Carpenter LJ, Archer SD, Beale R (2012) Ocean-atmosphere trace gas exchange. Chem Soc Rev 41:6473–6506
Carpenter LJ, Reimann S, Burkholder JB, Clerbaux C, Hall BD, Hossaini R, Laube JC, Yvon-Lewis SA (2014) Ozone-depleting substances (ODSs) and other gases of interest to the Montreal protocol. In: Scientific Assessment of Ozone Depletion: 2014, Global ozone research and monitoring project-report no.55. World Meteorological Organization, Geneva
Chance R, Baker AR, Küpper FC, Hughes C, Kloareg B, Malin G (2009) Release and transformations of inorganic iodine by marine macroalgae. Estuar Coast Shelf Sci 82:406–414
Chipperfield MP, Pyle JA (1998) Model sensitivity studies of Arctic ozone depletion. J Geophys Res 103:28389–28403
Collén J, Pedersén M (1999) Production, scavenging and toxicity of hydrogen peroxide in the green seaweed Ulva rigida. Eur J Phycol 31:265–271
Collén J, Ekdahl A, Abrahamsson K, Pédersen M (1994) The involvement of hydrogen peroxide in the production of volatile halogenated compounds by Meristiella gelidium. Phytochemistry 36:1197–1202
Collén J, Jimenez del Rio M, Garcia-Reina G, Pédersen M (1995) Photosynthetic production of hydrogen peroxide by Ulva rigida C. Ag. (Chlorophyta). Planta 196:225–230
Colvard NB, Carrington E, Helmuth B (2014) Temperature-dependent photosynthesis in the intertidal alga Fucus gardneri and sensitivity to ongoing climate change. J Exp Mar Biol Ecol 458:6–12
Daniel JS, Solomon S, Portmann RW, Garcia RR (1999) Stratospheric ozone destruction: the importance of bromine relative to chlorine. J Geophys Res 104:23871–23880
de Bettignies T, Wernberg T, Gurgel CFD (2018) Exploring the influence of temperature on aspects of the reproductive phenology of temperate seaweeds. Front Mar Sci 5:1–8
de Oliveira LS, Tschoeke DA, Magalhães Lopes ACR, Sudatti DB, Meirelles PM, Thompson CC, Pereira RC, Thompson FL (2017) Molecular mechanisms for microbe recognition and defense by the red seaweed Laurencia dendroidea. mSphere 2:e00094–e00017
Dessens O, Zeng G, Warwick N, Pyle J (2009) Short-lived bromine compounds in the lower stratosphere; impact of climate change on ozone. Atmos Sci Lett 10:201–206
Dietz KJ (2016) Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol Cell 39:20–25
Dummermuth AL, Karsten U, Fisch KM, König GM, Wiencke C (2003) Responses of marine macroalgae to hydrogen-peroxide stress. J Exp Mar Biol Ecol 289:103–121
Durack PJ, Wijffels SE, Matear RJ (2012) Ocean salinities reveal strong global water cycle intensification during 1950 to 2000. Science 336:455–458
Ekdahl A, Pédersen M, Abrahamsson K (1998) A study of the diurnal variation of biogenic volatile halocarbons. Mar Chem 63:1–8
FAO (2018) The global status of seaweed production, trade and utilization. Globefish Research Programme 124
Figueroa FL, Korbee N, Carrillo P, Medina-Sánchez JM, Mata MT, Bonomi J, Sánchez-Castillo PM (2009) The effects of UV radiation on photosynthesis estimated as chlorophyll fluorescence in Zygnemopsis decussata (Chlorophyta) growing in a high mountain lake (Sierra Nevada, southern Spain). J Limnol 68:206–216
Fuhlbrügge S, Quack B, Tegtmeier S, Atlas E, Hepach H, Shi Q, Raimund S, Krüger K (2016) The contribution of oceanic halocarbons to marine and free tropospheric air over the tropical West Pacific. Atmos Chem Phys 16:7569–7585
Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1991) Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentration. J Appl Phycol 3:355–362
Gao K, Aruga Y, Asada K, Kiyohara M (1993) Influence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J Appl Phycol 5:563–571
Goodwin KD, North WJ, Lidstrom ME (1997) Production of bromoform and dibromomethane by Giant kelp: factors affecting release and comparison to anthropogenic bromine sources. Limnol Oceanogr 42:1725–1734
Gordillo FJL (2012) Environment and algal nutrition. In: Wiencke C, Bischof K (eds) Seaweed biology. Springer, Berlin, pp 67–86
Gribble GW (2003) The diversity of naturally produced organohalogens. Chemosphere 52:289–297
Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH (2012) Effects of climate change on global seaweed communities. J Phycol 48:1064–1078
Hepach H, Quack B, Ziska F, Fuhlbrügge S, Atlas EL, Krüger K, Peeken I, Wallace DWR (2014) Drivers of diel and regional variations of halocarbon emissions from the tropical North East Atlantic. Atmos Chem Phys 14:1255–1275
Hepach H, Quack B, Raimund S, Fischer T, Atlas EL, Bracher A (2015) Halocarbon emissions and sources in the equatorial Atlantic cold tongue. Biogeosciences 12:6369–6387
Ho DT, Zappa CJ, McGillis WR, Bliven LF, Ward B, Dacey JWH, Schlosser P, Hendricks MB (2004) Influence of rain on air-sea gas exchange: Lessons from a model ocean. J Geophys Res 109:C08S18
Hoegh-Guldberg O, Cai R, Poloczanska ES, Brewer PG, Sundby S, Hilmi K, Fabry VJ, Jung S (2014) The Ocean. In: Barros VR, Field CB, Dokken DJ, Mastrandrea MD, Mach KJ, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York, pp 1655–1731
Hoegh-Guldberg, O, Jacob, D, Taylor, M, Bindi, M, Brown, S, Camilloni, I, Diedhiou, A, Djalante, R, Ebi, K.L, Engelbrecht, F, Guiot, J, Hijioka, Y, Mehrotra, S, Payne, A, Seneviratne, S.I, Thomas, A, Warren, R, Zhou, G, (2018). Impacts of 1.5°C global warming on natural and human systems. In: Masson-Delmotte V, Zhai P, Pörtner HO, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, Matthews JBR, Chen Y, Zhou X, Gomis MI, Lonnoy E, Maycock T, Tignor M, Waterfield T (eds) Global Warming of 1.5°C, An IPCC Special Report on the Impacts of Global Warming of 1.5°C Above Pre-industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty. In Press
Hopkins FE, Turner SM, Nightingale PD, Steinke M, Bakker D, Liss PS (2010) Ocean acidification and marine trace gas emissions. Proc Natl Acad Sci U S A 107:760–765
Hopkins FE, Kimmance SA, Stephens JA, Bellerby RGJ, Brussaard CPD, Czerny J, Schulz KG, Archer SD (2013) Response of halocarbons to ocean acidification in the Arctic. Biogeosciences 10:2331–2345
Hossaini R, Chipperfield MP, Dhomse S, Ordonez C, Saiz-Lopez A, Abraham NL, Archibald A, Braesicke P, Telford P, Warwick N, Yang X, Pyle J (2012) Modelling future changes to the stratospheric source gas injection of biogenic bromocarbons. Geophys Res Lett 39:L20813
Hossaini R, Chipperfield MP, Montzka SA, Rap A, Dhomse S, Feng W (2015) Efficiency of short-lived halogens at influencing climate through depletion of stratospheric ozone. Nat Geosci 8:186–190
Hossaini R, Patra PK, Leeson AA, Krysztofiak G, Abraham NL, Andrews SJ, Archibald AT, Aschmann J, Atlas EL, Belikov DA, Bönisch H, Carpenter LJ, Dhomse S, Dorf M, Engel A, Feng W, Fuhlbrügge S, Griffiths PT, Harris NRP, Hommel R, Keber T, Krüger K, Lennartz ST, Maksyutov S, Mantle H, Mills GP, Miller B, Montzka SA, Moore F, Navarro MA, Oram DE, Pfeilsticker K, Pyle JA, QuackB RAD, Saikawa E, Saiz-Lopez A, Sala S, Sinnhuber BM, Taguchi S, Tegtmeier S, Lid-ster RT, Wilson C, Ziska F (2016) A multi-model intercomparison of halogenated very short-lived substances (TransCom- VSLS): linking oceanic emissions and tropospheric transport for a reconciled estimate of the stratospheric source gas injection of bromine. Atmos Chem Phys 16:9163–9187
IPCC (2018) Summary for Policymakers. In: Masson-Delmotte V, Zhai P, Pörtner HO, Roberts D, Skea J, Shukla PR, Pirani A, Moufouma-Okia W, Péan C, Pidcock R, Connors S, JBR M, Chen Y, Zhou X, Gomis MI, Lonnoy E, Maycock T, Tignor M, Waterfield T (eds) Global warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. World Meteorological Organization, Geneva, Switzerland
Keng FSL, Phang SM, Abd Rahman N, Leedham EC, Hughes C, Robinson AD, Harris NRP, Pyle JA, Sturges WT (2013) Volatile halocarbon emissions by three tropical brown seaweeds under different irradiances. J Appl Phycol 25:1377–1386
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328
Krenn BE, Plat H, Wever R (1987) The bromoperoxidase from the red alga Ceramium rubrum also contains vanadium as a prosthetic group. Biochim Biophys Acta Protein Struct Mol Enzymol 912:287–291
Küpper FC, Schweigert N, Ar Gall E, Legendre JM, Vilter H, Kloareg B (1998) Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta 207:163–171
Küpper FC, Kloareg B, Guern J, Potin P (2001) Oligoguluronates elicit an oxidative burst in the brown algal kelp. Plant Physiol 125:278–291
Küpper FC, Müller DG, Peters AF, Kloareg B, Potin P (2002) Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J Chem Ecol 28:2057–2081
Küpper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite TJ, Boneberg EM, Woitsch S, Weiller M, Abela R, Grolimund D, Potin P, Butler A, Luther GW 3rd, Kroneck PM, Meyer-Klaucke W, Feiters MC (2008) Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad Sci U S A 105:6954–6958
Küpper FC, Feiters MC, Olofsson B, Kaiho T, Yanagida S, Zimmermann MB, Carpenter LJ, Luther GW III, Lu Z, Jonsson M, Kloo L (2011) Commemorating two centuries of iodine research: An interdisciplinary overview of current research. Angew Chemie Internat Edn 50:11598–11620
Küpper FC, Carpenter LJ, Leblanc C, Toyama C, Uchida Y, Maskrey BJ, Robinson J, Verhaeghe EF, Malin G, Luther GW III, Kroneck PMH, Kloareg B, Meyer-Klaucke W, Muramatsu Y, Megson IK, Potin P, Feiters MC (2013) In vivo speciation studies and antioxidant properties of bromine in Laminaria digitate reinforce the significance of iodine accumulation for kelps. J Exp Bot 64:2653–2664
Küpper FC, Leblanc C, Meyer-Klaucke W, Potin P, Feiters MC, Amsler C (2014) Different speciation for bromine in brown and red algae, revealed by in vivo X-ray absorption spectroscopic studies. J Phycol 50:652–664
Küpper FC, Miller EP, Andrews SJ, Hughes C, Carpenter LJ, Meyer-Klaucke W, Toyama C, Muramatsu Y, Feiters MC, Carrano CJ (2018) Emission of volatile halogenated compounds, speciation and localization of bromine and iodine in the brown algal genome model Ectocarpus siliculosus. J Biol Inorg Chem 23:1119–1128
Laturnus F (1995) Release of volatile halogenated organic compounds by unialgal cultures of polar macroalgae. Chemosphere 31:3387–3395
Laturnus F (2001) Marine macroalgae in polar regions as natural sources for volatile organohalogens. Environ Sci Pollut Res 8:103–108
Laturnus F, Wiencke C, Adams FC (1998) Influence of light conditions on the release of volatile halocarbons by Antarctic macroalgae. Mar Environ Res 45:285–294
Laturnus F, Giese B, Wiencke C, Adams FC (2000) Low-molecular-weight organoiodine and organobromine compounds released by polar macroalgae – the influence of abiotic factors. Fresenius J Anal Chem 368:297–302
Laturnus F, Svensson T, Wiencke C (2010) Release of reactive organic halogens by the brown macroalga Saccharina latissima after exposure to ultraviolet radiation. Polar Res 29:379–384
Leedham Elvidge EC, Phang SM, Sturges WT, Malin G (2015) The effect of desiccation on the emission of volatile bromocarbons from two common temperate macroalgae. Biogeosci Discuss 11:10673–10701
Leedham EC, Hughes C, Keng FSL, Phang SM, Malin G, Sturges WT (2013) Emission of atmospherically significant halocarbons by naturally occurring and farmed tropical macroalgae. Biogeosciences 10:3615–3633
Liang Q, Atlas E, Blake D, Dorf M, Pfeilsticker K, Schauffler S (2014) Convective transport of very-short-lived bromocarbons to the stratosphere. Atmos Chem Phys 14:5781–5792
Lin CY, Manley SL (2012) Bromoform production from seawater treated with bromoperoxidase. Limnol Oceanogr 57:1857–1866
Liu Y, Thornton DCO, Bianchi TS, Arnold WA, Shields MR, Chen J, Yvon-Lewis SA (2015) Dissolved organic matter composition drives the marine production of brominated very short-lived substances. Environ Sci Technol 49:3366–3374
Manley SL (2002) Phytogenesis of halomethanes: a product of selection or a metabolic accident? Biogeochemistry 60:163–180
Manley SL, Barbero PE (2001) Physiological constraints on bromoform (CHBr3) production by Ulva lactuca (Chlorophyta). Limnol Oceanogr 46:1392–1399
Milkova T, Talev G, Christov R, Dimitrova-Konaklieva S, Popov S (1997) Sterols and volatiles in Cystoseira barbata and Cystoseira crinita from the Black Sea. Phytochemistry 45:93–95
Mithoo-Singh PK, Keng FSL, Phang SM, Leedham Elvidge EC, Sturges WT, Malin G, Abd Rahman N (2017) Halocarbon emissions by selected tropical seaweeds, species-specific and compound-specific responses under changing pH. PeerJ 5:e2918
Mtolera MSO, Collén J, Pedersén M, Ekdahl A, Abrahamsson K, Semesi AK (1996) Stress-induced production of volatile halogenated organic compounds in Eucheuma denticulatum (Rhodophyta) caused by elevated pH and high light intensities. Eur J Phycol 31:89–95
Neilson AH (2003) Biological effects and biosynthesis of brominated metabolites. In: Neilson AH (ed) The handbook of environmental chemistry vol 3. Springer, Berlin, pp 75–204
Nightingale PD, Malin G, Liss PS (1995) Production of chloroform and other low-molecular-weight halocarbons by some species of macroalgae. Limnol Oceanogr 40:680–689
Ohsawa N, Ogata Y, Okada N, Itoh N (2001) Physiological function of bromoperoxidase in the red marine alga, Corallina pilulifera: production of bromoform as an allelochemical and the simultaneous elimination of hydrogen peroxide. Phytochemistry 58:683–692
Opsahl S, Benner R (1997) Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 6:480–482
Palmer CJ, Anders TL, Carpenter LJ, Küpper FC, McFiggans G (2005) Iodine and halocarbon response of Laminaria digitata to oxidative stress and links to atmospheric new particle production. Environ Chem 2:282–290
Paul C, Pohnert G (2011) Production and role of volatile halogenated compounds from marine algae. Nat Prod Rep 28:186–194
Paul NA, de Nys R, Steinberg PD (2006) Chemical defense against bacteria in the red alga Asparagopsis armata: linking structure with function. Mar Ecol Prog Ser 306:87–101
Pedersén M, Collén J, Abrahamsson K, Ekdahl A (1996) Production of halocarbons from seaweeds: an oxidative stress reaction? Sci Mar 60:255–261
Phang SM, Keng FSL, Mithoo-Singh PK, Lim YK, Abd Rahman N, Leedham EC, Robinson AD, Harris NRP, Pyle JA, Sturges WT (2015) Can seaweed farming in the tropics contribute to climate change through emission of short-lived halocarbons? Malays J Sci 34:7–18
Potin P (2008) Oxidative burst and related responses in biotic interactions in algae. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 245–271
Punitha T, Phang SM, Juan JC, Beardall J (2017) Environmental control of vanadium haloperoxidases and halocarbon emissions in macroalgae. Mar Biotechnol 20:282–303
Quack B, Wallace DWR (2003) Air-sea flux of bromoform: controls, rates and implications. Glob Biogeochem Cycles 17:1023–1050
Quack B, Atlas E, Petrick G, Wallace DWR (2007) Bromoform and dibromomethane above the mauritanian upwelling: atmospheric distributions and oceanic emissions. J Geophys Res-Atmos 112:D09312
Rabalais NN, Turner RE, Díaz RJ, Justić D (2009) Global change and eutrophication of coastal waters. ICES J Mar Sci 66:1528–1537
Raikar SV, Lima M, Fujita Y (2001) Effect of temperature, salinity and light intensity on the growth of Gracilaria spp. (Gracilariales, Rhodophyta) from Japan, Malaysia and India. Indian J Mar Sci 30:98–104
Raimund S, Quack B, Bozec Y, Vernet M, Rossi V, Garçon V, Morel Y, Morin P (2011) Sources of short-lived bromocarbons in the Iberian upwelling system. Biogeosciences 8:1551–1564
Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett 586:603–616
Saiz-Lopez A, Plane JMC, Baker AR, Carpenter LJ, von Glasow R, Martín JCG, McFiggans G, Saunders RW (2011) Atmospheric chemistry of Iodine. Chem Rev 112 :1773–1804
Satoh H, Nakamura Y, Okabe S (2007) Influences of infaunal burrows on the community structure and activity of ammonia-oxidizing bacteria in intertidal sediments. Appl Environ Microbiol 73:1341–1348
Stemmler I, Hense I, Quack B (2015) Marine sources of bromoform in the global open ocean – global patterns and emissions. Biogeosciences 12:1967–1981
Stewart RIA, Dossena M, Bohan DA, Jeppesen E, Kordas RL, Ledger ME, Meerhoff M, Moss B, Mulder C, Shurin JB, Suttle B, Thompson R, Trimmer M, Woodward G (2013) Mesocosm experiments as a tool for ecological-climate change research. Adv Ecol Res 48:71–181
Sundström J, Collén J, Abrahamsson K, Pedersén M (1996) Halocarbon production ad in vivo brominating activity of Eucheuma denticulatum. Phytochemistry 42:15527–11530
Sung MS, Hsu YT, Wu TM, Lee TM (2009) Hypersalinity and hydrogen peroxide upregulation of gene expression of antioxidant enzymes in Ulva fasciata against oxidative stress. Mar Biotechnol 11:199–209
Tadaaki B, Muramatsu Y, Amachi S (2006) Rate of iodine volatilization and accumulation by filamentous fungi through laboratory cultures. Chemosphere 65:2216–2222
Tegtmeier S, Kruger K, Quack B, Atlas EL, Pisso I, Stohl A, Yang X (2012) Emission and transport of bromocarbons: from the West Pacific Ocean into the stratosphere. Atmos Chem Phys 12:10633–10648
Thornton DCO (2014) Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur J Phycol 49:20–46
Toda H, Itoh N (2011) Isolation and characterization of gene encoding S-adenosyl-L-methionine-dependent halide/thiol methyltransferase (HTMT) from marine diatom Phaeodactylum tricornutum: biogenic emissions of CH3I emissions in oceans. Phytochemistry 72:337–343
Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434
Tropin IV, Radzinskaya NV, Voskoboinikov GM (2003) The influence of salinity on the rate of dark respiration and structure of the cells of brown algae thalli from the Barents Sea littoral. Biol Bull 30:40–47
van Vuuren DP, Edmonds J, Kainuma MLT, Riahi K, Thomson A, Matsui T, Hurtt G, Lamarque JF, Meinshausen M, Smith S, Grainer C, Rose S, Hibbard KA, Nakicenovic N, Krey V, Kram T (2011) Representative concentration pathways: An overview. Clim Chang 109:5–31
Verhaeghe EF, Fraysse A, Guerquin-Kern JL, Wu TD, Devès G et al (2008) Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. J Biol Inorg Chem 13:257–269
Webb AL, Leedham Elvidge E, Hughes C, Hopkins FE, Malin G, Bach LT, Schulz K, Crawfurd K, Brussaard CPD, Stuhr A, Riebesell U, Liss PS (2016) Effect of ocean acidification and elevated fCO2 on trace gas production by a Baltic Sea summer phytoplankton community. Biogeosciences 13:4595–4613
Weinberg I, Bahlmann E, Eckhardt T, Michaelis W, Seifert R (2015) A halocarbon survey from a seagrass dominated subtropical lagoon, Ria Formosa (Portugal): flux pattern and isotopic composition. Biogeosciences 12:1697–1711
Weinberger F, Coquempot B, Forner S, Morin P, Kloareg B, Potin P (2007) Different regulation of haloperoxidation during agar oligosaccharide-activated defence mechanisms in two related red algae, Gracilaria sp and Gracilaria chilensis. J Exp Bot 58:4365–4372
Wever R, van der Horst MA (2013) The role of vanadium haloperoxidases in the formation of volatile brominated compounds and their impact on the environment. Dalton Trans 42:11778–11786
Wever R, Tromp MGM, Krenn BE, Marjani A, Van Toi M (1991) Brominating activity of seaweed Ascophyllum nodosum: impact on the biosphere. Environ Sci Technol 25:446–449
White AL, Jahnke LS (2002) Contrasting effects of UV-A and UV-B on photosynthesis and photoprotection of b-carotene in two Dunaliella spp. Plant Cell Physiol 43:877–884
WMO (World Meteorological Organization) (2018) Scientific Assessment of Ozone Depletion: 2018, Global Ozone Research and Monitoring Project–Report No.58. World Meteorological Organisation, Geneva
Wong SL, Chang J (2000) Salinity and light effects on growth, photosynthesis, and respiration of Grateloupia filicina (Rhodophyta). Aquaculture 182:387–395
Wood HL, Widdicombe S, Spicer JI (2009) The influence of hypercapnia and the infaunal brittlestar Amphiura filiformis on sediment nutrient flux – will ocean acidification affect nutrient exchange? Biogeosciences 6:2015–2024
Xu D, Brennan G, Xu L, Zhang XW, Fan X, Han WT, Mock T, McMinn A, Hutchins DA, Ye NH (2019) Ocean acidification increases iodine accumulation in kelp-based coastal food webs. Glob Chang Biol 25:629–639
Xue LG, Zhang Y, Zhang TG, An LZ, Wang XL (2005) Effects of enhanced ultraviolet-B radiation on algae and cyanobacteria. Crit Rev Microbiol 31:79–89
Yakovleva IM, Belotsitsenko ES (2017) The antioxidant potential of dominant macroalgae species from the Sea of Japan. Russ J Mar Biol 43:407–418
Yamamoto H, Yokouchi Y, Otsuki A, Itoh H (2001) Depth profiles of volatile halogenated hydrocarbons in seawater in the bay of Bengal. Chemosphere 45:371–377
Yokouchi Y, Osada K, Wada M, Hasebe F, Agama M, Murakami R, Mukai H, Nojiri Y, Inuzuka Y, Toom-Sauntry D, Fraser P (2008) Global distribution and seasonal concentration change of methyl iodide in the atmosphere. J Geophys Res 113 (D18)
Yokouchi Y, Ooki A, Hashimoto S, Itoh N (2014) A study on the production and emission of marine-derived volatile halocarbons. In: Uematsu M, Yokouchi Y, Watanabe YW, Takeda S, Yamanaka Y (eds) Western Pacific air-sea interaction study. TERRAPUB, Tokyo, pp 1–25
Younus H (2018) Therapeutic potentials of superoxide dismutase. Int J Health Sci 12:88–93
Zark M, Riebesell U, Dittmar T (2015) Effects of ocean acidification on marine dissolved organic matter are not detectable over the succession of phytoplankton blooms. Sci Adv 1:e1500531
Ziska F, Quack B, Abrahamsson K, Archer SD, Atlas E et al (2013) Global sea-to-air flux climatology for bromoform, dibromomethane and methyl iodide. Atmos Chem Phys 13:8915–8934
Ziska F, Quack B, Tegtmeier S, Stemmler I, Krüger K (2017) Future emissions of marine halogenated very-short lived substances under climate change. J Atmos Chem 74:245–260
Zou DH, Gao KS (2014) Temperature response of photosynthetic light and carbon-use characteristics in the red seaweed Gracilariopsis lemaneiformis (Gracilariales, Rhodophyta). J Phycol 50:366–375
Zou XX, Xing SS, Su X, Zhu J, Huang HQ, Bao SX (2018) The effects of temperature, salinity and irradiance upon the growth of Sargassum polycystum C. Agardh (Phaeophyceae). J Appl Phycol 30:1207–1215
Funding
This research was funded by the Phase II Higher Institution Centre of Excellence (HICoE) Fund, the Ministry of Education Malaysia (IOES-2014F), University of Malaya Top 100 Research University Grant (TU001D-2018) and the University of Malaya Postgraduate Research Funds, PPP (PG300-2016A).
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Keng, F.SL., Phang, SM., Abd Rahman, N. et al. The emission of volatile halocarbons by seaweeds and their response towards environmental changes. J Appl Phycol 32, 1377–1394 (2020). https://doi.org/10.1007/s10811-019-02026-x
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DOI: https://doi.org/10.1007/s10811-019-02026-x