Skip to main content

Advertisement

SpringerLink
Log in

Molecular iodine emission rates and photosynthetic performance of different thallus parts of Laminaria digitata (Phaeophyceae) during emersion

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The emission of molecular iodine (I2) from the stipe, the meristematic area and the distal blade of the brown macroalga Laminaria digitata (Hudson) Lamouroux (Phaeophyceae) was monitored under low light and dark conditions. Photosynthetic parameters were determined to investigate both the extent of stress experienced by different thallus parts and the effects of emersion on photosynthesis. Immediately after air exposure, intense I2 emission was detectable from all thallus parts. I2 emission declined continuously over a period of 180 min following the initial burst, but was not affected by the light regime. The total number of mole of I2 emitted by stipes was approximately 10 times higher than those emitted from other thallus parts. Initial I2 emission rates (measured within 30 min of exposure to air) were highest for stipes (median values: 2,999 and 5,222 pmol g−1 dw min−1 in low light and dark, respectively) and lower, by one order of magnitude, for meristematic regions and distal blades. After exposure to air for between 60 and 180 min, I2 emission rates of all thallus parts were reduced by 70–80%. Air exposure resulted in a decrease of the maximum photosystem II (PSII) efficiency (F v/F m) by 3%, and in a 25–55% increase of the effective PSII quantum efficiency (\( \Updelta F/F^{\prime}_{\text{m}} \)); this was caused by a higher fraction of open reaction centres (qP), whereas the efficiency of the latter in capturing energy (\( F^{\prime}_{\text{v}} /F^{\prime}_{\text{m}} \)) remained constant. The results indicate the presence of an iodine pool which is easily volatilised and depleted due to air exposure, even under apparently low stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

IBBCEAS:

Incoherent broadband cavity-enhanced absorption spectroscopy

HWHM:

Half-width at half-maximum

MBL:

Marine boundary layer

NPQ:

Non-photochemical quenching

PFD:

Photon flux density

PAR:

Photosynthetic active radiation

PS:

Photosystem

References

  • Amat MA, Srivastava LM (1985) Translocation of iodine in Laminaria saccharina (Phaeophyta). J Phycol 21:330–333

    Article  CAS  Google Scholar 

  • Ar Gall E, Küpper FC, Kloareg B (2004) A survey of iodine content in Laminaria digitata. Bot Mar 47:30–37

    Article  CAS  Google Scholar 

  • Bale CSE, Ingham T, Commane R, Heard DE, Bloss WJ (2008) Novel measurements of atmospheric iodine species by resonance fluorescence. J Atmos Chem 60:51–70

    Article  CAS  Google Scholar 

  • Ball SM, Hollingsworth SA, Humbles J, Leblanc C, Potin P, McFiggans G (2010) Spectroscopic studies of molecular iodine emitted into the gas phase by seaweed. Atmos Chem Phys 10:6237–6254

    Article  CAS  Google Scholar 

  • Bitter M, Ball SM, Povey IM, Jones RL (2005) A broadband cavity ringdown spectrometer for in situ measurements of atmospheric trace gases. Atmos Chem Phys 5:2547–2560

    Article  CAS  Google Scholar 

  • Büchel C, Wilhelm C (1993) In vivo analysis of slow fluorescence induction kinetics in algae: progress, problems and perspectives. J Photochem Photobiol 58:137–148

    Article  Google Scholar 

  • Carpenter LJ (2003) Iodine in the marine boundary layer. Chem Rev 103:4953–4962

    Article  PubMed  CAS  Google Scholar 

  • Dethier MN, Williams SL (2009) Seasonal stresses shift optimal intertidal algal habitats. Mar Biol 156:555–567

    Article  Google Scholar 

  • Dixneuf S, Ruth AA, Vaughan S, Varma RM, Orphal J (2009) The time dependence of molecular iodine emission from Laminaria digitata. Atmos Chem Phys 9:823–829

    Article  CAS  Google Scholar 

  • Dring MJ, Brown FA (1982) Photosynthesis of intertidal brown algae during and after periods of emersion: a renewed search for physiological causes of zonation. Mar Ecol Prog Ser 8:301–308

    Article  Google Scholar 

  • Evans LV, Holligan MS (1972) Correlated light and electron microscope studies on brown algae. II. Physode production in Dictyota. New Phytol 71:1173–1180

    Article  Google Scholar 

  • Fiedler SE, Hese A, Ruth AA (2003) Incoherent broad-band cavity-enhanced absorption spectroscopy. Chem Phys Lett 371:284–294

    Article  CAS  Google Scholar 

  • Garbary DJ, Kim KY (2005) Anatomical differentiation and photosynthetic adaptation in brown algae. Algae 20:233–238

    Article  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Gevaert F, Creach A, Davoult D, Holl AC, Seuront L, Lemoine Y (2002) Photo-inhibition and seasonal photosynthetic performance of the seaweed Laminaria saccharina during a simulated tidal cycle: chlorophyll fluorescence measurements and pigment analysis. Plant Cell Environ 25:859–872

    Article  CAS  Google Scholar 

  • Gómez I, López-Figueroa F, Ulloa N, Morales V, Lovengreen C, Huovinen P, Hess S (2004) Patterns of photosynthesis in 18 species of intertidal macroalgae from southern Chile. Mar Ecol Prog Ser 270:103–116

    Article  Google Scholar 

  • Harker M, Berkaloff C, Lemoine Y, Britton G, Young A, Duval JC, Rmiki N-E, Rousseau B (1999) Effects of high light and desiccation on the operation of the xanthophyll cycle in two marine brown algae. Eur J Phycol 34:35–42

    Article  Google Scholar 

  • Haug A, Jensen A (1954) Seasonal variations in the chemical composition of Alaria esculenta, Laminaria saccharina, Laminaria hyperborea and Laminaria digitata from northern Norway. Norwegian Institute of Seaweed Research, Report no. 84, p 34

  • Hou X, Hansena V, Aldahanb A, Possnert G, Lindd OC, Lujaniene G (2009) A review on speciation of iodine-129 in the environmental and biological samples. Anal Chim Acta 632:181–196

    Article  PubMed  CAS  Google Scholar 

  • Huang RJ, Seitz K, Buxmann J, Pöhler D, Hornsby KE, Carpenter LJ, Platt U, Hoffmann T (2010) In situ measurements of molecular iodine in the marine boundary layer: the link to macroalgae and the implications for O3, IO, OIO and NO x . Atmos Chem Phys 10:4823–4833

    Article  CAS  Google Scholar 

  • Hunt LJH, Denny MW (2008) Desiccation protection and disruption: a trade-off for an intertidal marine alga. J Phycol 44:1164–1170

    Article  Google Scholar 

  • Johnson WS, Gigon A, Gulmon SL, Mooney HA (1974) Comparative photosynthetic capacities of intertidal algae under exposed and submerged conditions. Ecology 55:450–453

    Article  Google Scholar 

  • Kolb CE (2002) Iodine’s air of importance. Nature 417:597–598

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Küpper FC, Kloareg B, Guern J, Potin P (2001) Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol 125:278–291

    Article  PubMed  Google Scholar 

  • Küpper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite TJ, Boneberg E-M, Woitsch S, Weiller M, Abela R, Grolimund D, Potin P, Butler A, Luther GW, Kroneck PMH, Meyer-Klaucke W, Feiters MC (2008) Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad Sci USA 105:6954–6958

    Article  PubMed  Google Scholar 

  • Kylin H (1929) Über das Vorkommen von Jodiden, Bromiden und Jodidoxidasen bei den Meeresalgen. Hoppe-Seylor’s Z Physiol Chem 186:50–84

    Article  CAS  Google Scholar 

  • Laturnus F, Svensson T, Wiencke C, Öberg G (2004) Ultraviolet radiation affects emission of ozone-depleting substances by marine macroalgae: results from a laboratory incubation study. Environ Sci Technol 38:6605–6609

    Article  PubMed  CAS  Google Scholar 

  • Leblanc C, Colin C, Cosse A, Delage L, La Barre S, Morin P, Fiévet B, Voiseux C, Ambroise Y, Verhaeghe E, Amouroux D, Donard O, Tessier E, Potin P (2006) Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie 88:1773–1785

    Article  PubMed  CAS  Google Scholar 

  • Linger P, Brüggemann W (1999) Correlations between chlorophyll fluorescence quenching parameters and photosynthesis in a segregating Lycopersicon esculentum × L. peruvianum population as measured under constant conditions. Photosynth Res 61:145–156

    Article  CAS  Google Scholar 

  • Lobban CS, Harrisson PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Lüning K (1985) Meeresbotanik. Gustav Thieme Verlag, Stuttgart

    Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence − a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • McFiggans G, Coe H, Burgess R, Allan J, Cubison M, Alfarra MR, Saunders R, Saiz-Lopez A, Plane JMC, Wevill DJ, Carpenter LJ, Rickard AR, Monks PS (2004) Direct evidence for coastal iodine particles from Laminaria macroalgae – linkage to emissions of molecular iodine. Atmos Chem Phys 4:701–713

    Article  CAS  Google Scholar 

  • McFiggans G, Bale CSE, Ball SM, Beames JM, Bloss WJ, Carpenter LJ, Dorsey J, Dunk R, Flynn MJ, Furneaux KL, Gallagher MW, Heard DE, Hollingsworth AM, Hornsby K, Ingham T, Jones CE, Jones RL, Kramer LJ, Langridge JM, Leblanc C, LeCrane JP, Lee JD, Leigh RJ, Longley I, Mahajan AS, Monks PS, Oetjen H, Orr-Ewing AJ, Plane JMC, Potin P, Shillings AJL, Thomas F, von Glasow R, Wada R, Whalley LK, Whitehead JD (2010) Iodine-mediated coastal particle formation: an overview of the Reactive Halogens in the Marine Boundary Layer (RHaMBLe) Roscoff coastal study. Atmos Chem Phys 10:2975–2999

    Article  CAS  Google Scholar 

  • O’Dowd CD, Hoffmann T (2005) Coastal new particle formation: a review of the current state-of-the-art. Environ Chem 2:245–255

    Article  Google Scholar 

  • O’Dowd CD, Jimenez JL, Bahreini R, Flagan RC, Seinfeld JH, Hameri K, Pirjola L, Kulmala M, Jennings SG, Hoffmann T (2002) Marine aerosol formation from biogenic iodine emissions. Nature 417:632–636

    Article  PubMed  Google Scholar 

  • Palmer CJ, Anders TL, Carpenter LJ, Küpper FC, McFiggans GB (2005) Iodine and halocarbon response of Laminaria digitata to oxidative stress and links to atmospheric new particle production. Environ Chem 2:282–290

    Article  CAS  Google Scholar 

  • Pedersén M, Roomans GM (1983) Ultrastructural localization of bromine and iodine in the stipes of Laminaria digitata (Huds.) Lamour., Laminaria saccharina (L.) Lamour. and Laminaria hyperborea (Gunn.) Fosl. Bot Mar 26:113–118

    Article  Google Scholar 

  • Saenko GN, Kravtsova YY, Ivanenko VV, Sheludko SI (1978) Concentration of iodine and bromine by plants in seas of Japan and Okhotsk. Mar Biol 47:243–250

    Article  Google Scholar 

  • Saiz-Lopez A, Plane JMC (2004) Novel iodine chemistry in the marine boundary layer. Geophys Res Lett 31:L04112

    Article  Google Scholar 

  • Saiz-Lopez A, Saunders RW, Joseph DM, Ashworth SH, Plane JMC (2004) Absolute absorption cross-section and photolysis rate of I2. Atmos Chem Phys 4:1443–1450

    Article  CAS  Google Scholar 

  • Schonbeck M, Norton TA (1978) Factors controlling upper limits of fucoid algae on shore. J Exp Mar Biol Ecol 31:303–313

    Article  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Seitz K, Buxmann J, Pöhler D, Sommer T, Tschritter J, Neary T, O’Dowd C, Platt U (2010) The spatial distribution of the reactive iodine species IO from simultaneous active and passive DOAS observations. Atmos Chem Phys 10:2117–2128

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman, New York

    Google Scholar 

  • van den Hoek C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, Cambridge

    Google Scholar 

  • Verhaeghe E, Fraysse A, Guerquin-Kern J-L, Wu T-D, Devès G, Mioskowski C, Leblanc C, Ortega R, Ambroise Y, Potin P (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

    Article  PubMed  CAS  Google Scholar 

  • Wiltens J, Schreiber U, Vidaver W (1978) Chlorophyll fluorescence induction – indicator of photosynthetic activity in marine algae undergoing desiccation. Can J Bot Rev Can Bot 56:2787–2794

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Professor Colin O’Dowd (School of Physics and Ryan Institute, NUI Galway), Dr. Solène Connan (Botany and Plant Science and Ryan Institute, NUI Galway) and Dr. Stewart Vaughan (School of Chemistry, University of Leeds, UK) for comments on the experimental design and Dr. Jerome Sheahane (Statistics and Applied Mathematics, School of Mathematics, NUI Galway) for his help with statistical analyses. UN and SD gratefully appreciate financial support through the Irish Research Council for Science, Engineering and Technology (IRCSET ‘Embark Initiative’).

Author information

Author notes

  1. Sophie Dixneuf

    Present address: Institut für Energie und Klimaforschung, IEK-8: Troposphäre, Forschungszentrum Jülich GmbH, 52425, Jülich, Germany

Authors and Affiliations

  1. Botany and Plant Science, School of Natural Sciences, Ryan Institute for Environmental, Marine and Energy Research, National University of Ireland Galway, Galway, Ireland

    Udo Nitschke & Dagmar B. Stengel

  2. Department of Physics, University College Cork, Cork, Ireland

    Albert A. Ruth & Sophie Dixneuf

  3. Environmental Research Institute, University College Cork, Cork, Ireland

    Albert A. Ruth & Sophie Dixneuf

Authors
  1. Udo Nitschke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Albert A. Ruth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sophie Dixneuf
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dagmar B. Stengel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sophie Dixneuf.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 42.6 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nitschke, U., Ruth, A.A., Dixneuf, S. et al. Molecular iodine emission rates and photosynthetic performance of different thallus parts of Laminaria digitata (Phaeophyceae) during emersion. Planta 233, 737–748 (2011). https://doi.org/10.1007/s00425-010-1334-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1334-3

Keywords

Search

Navigation