Skip to main content

The Peculiar Features of Non-Photochemical Fluorescence Quenching in Diatoms and Brown Algae

  • Chapter
  • First Online:
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 40))

Summary

Diatoms and brown algae are major contributors to marine primary production. They are biologically diverse, with thousands of different species, and are extremely successful, occupying almost every marine ecosystem ranging from the coastal-estuarine to deep-sea regions. Their ecological success is based in part on their ability to rapidly regulate photosynthesis in response to pronounced fluctuations in their natural light environment. Regulation of light harvesting, and the use of excitation energy, is largely based on effective dissipation of excessive energy as heat. Thermal dissipation of excitation energy is assessed as non-photochemical quenching of chlorophyll a fluorescence (NPQ). NPQ depends strongly on the conversion of xanthophylls: diadinoxanthin (Dd) to diatoxanthin (Dt) in the Dd-Dt cycle of diatoms and violaxanthin (V) to zeaxanthin (Z), via the intermediate antheraxanthin (A), in the VAZ cycle present in brown algae. Xanthophyll cycle (XC)-dependent thermal energy dissipation underlying NPQ represents one of the most important photoprotection mechanisms of diatoms and brown algae. In the present chapter, we review the biochemistry of XC enzymes with a special focus on co-substrate requirements and regulation of enzyme activity. In addition, we present a new model for the structural basis of XC-dependent NPQ in diatoms based on the latest experimental findings. In the last section, we highlight the importance of XC-dependent photoprotection for the ecological success of diatoms and brown algae in their natural environments.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

A –:

Antheraxanthin;

Asc –:

Ascorbate;

Chl a – :

Chlorophyll a;

Chl a 710−712 – :

Chlorophyll a fluorescence emission band between 710 and 712 nm;

Dd –:

Diadinoxanthin;

DDE –:

Diadinoxanthin de-epoxidase;

DEP –:

Diatoxanthin epoxidase;

DES –:

Diadinoxanthin de-epoxidation state;

Dt –:

Diadinoxanthin;

DTT –:

Dithiothreitol;

FCP –:

Fucoxanthin chlorophyll protein;

FCPa, FCPb, FCPo, Fcp6 –:

Fucoxanthin chlorophyll protein complex ‘a’, fucoxanthin chlorophyll protein complex ‘b’, fucoxanthin chlorophyll protein complex ‘o’, fucoxanthin chlorophyll protein ‘6’ (=Lhcx1);

H+ –:

Protons;

HII – :

MGDG inverted hexagonal phase;

LHC –:

Light-harvesting complex;

LHC7, LHC8 –:

Light-harvesting complex protein ‘7’, light-harvesting complex protein ‘8’;

Lhcf, Lhcx –:

Light-harvesting complex protein binding fucoxanthin, light-harvesting complex protein ‘x’;

LHCSR –:

Stress-related light-harvesting complex protein (=LI818);

LI818 –:

Light-induced light-harvesting complex protein ‘818’;

MGDG –:

Monogalactosyldiacylgycerol;

MPB –:

Microphytobenthic;

Ndh –:

NAD(P)H dehydrogenase;

NPQ –:

Non-photochemical quenching of chlorophyll fluorescence;

OEC –:

Oxygen evolving complex;

PQ –:

Plastoquinone;

PS II –:

Photosystem II;

PS II RC –:

Photosystem II reaction center;

Q1 and Q2 –:

Quenching sites 1 and 2;

qE –:

‘Energy- or pH-dependent’ quenching;

qI –:

‘Photoinhibitory’ quenching;

qT –:

‘State-transition’ quenching;

SQDG –:

Sulfoquinovosyldiacylglycerol;

V –:

Violaxanthin;

VDE –:

Violaxanthin de-epoxidase;

XC –:

Xanthophyll cycle;

Z –:

Zeaxanthin;

ZEP –:

Zeaxanthin epoxidase;

Δ522 nm –:

Absorption change at 522 nm;

ΔpH –:

Transthylakoid proton gradient;

References

  • Adams WW III, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186:390–398

    CAS  PubMed  Google Scholar 

  • Alderkamp A-C, de Baar HJW, Wisser RJW, Arrigo KR (2010) Can photoinhibition control phytoplankton abundance in deeply mixed water columns of the Southern Ocean? Limnol Oceanogr 55:1248–1264

    CAS  Google Scholar 

  • Apprill AM, Lesser MP (2003) Effects of ultraviolet radiation on Laminaria saccharina in relation to depth and tidal height in the Gulf of Maine. Mar Ecol Prog Ser 256:75–85

    CAS  Google Scholar 

  • Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192

    CAS  PubMed  Google Scholar 

  • Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21:2036–2044

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bailleul B, Rogato A, de Martino A, Coesel S, Cardol P, Bowler C, Falciatore A, Finazzi G (2010) An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc Natl Acad Sci USA 107:18214–18219

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blanchard G, Guarini J-M, Dang C, Richard P (2004) Characterizing and quantifying photoinhibition in intertidal microphytobenthos. J Phycol 40:692–696

    Google Scholar 

  • Brunet C, Lavaud J (2010) Can the xanthophyll cycle help extract the essence of the microalgal functional response to a variable light environment? J Plankton Res 32:1609–1617

    Google Scholar 

  • Brunet C, Johnsen G, Lavaud J, Roy S (2011) Pigments and photoacclimation processes. In: Roy S, Llewellyn CA, Skarstad E, Johnsen G (eds) Phytoplankton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography. Cambridge University Press, Cambridge, pp 445–471

    Google Scholar 

  • Carnicas E, JimĂ©nez C, Niell F (1999) Effects of changes of irradiance on the pigment composition of Gracilaria tenuistipitata var. liui Zhang et Xia. J Photochem Photobiol B 50:149–158

    CAS  Google Scholar 

  • Cartaxana P, Ruivo M, Hubas C, Davidson I, SerĂ´dio J, Jesus B (2011) Physiological versus behavioral photoprotection in intertidal epipelic and epipsammic benthic diatom communities. J Exp Mar Biol Ecol 405:120–127

    Google Scholar 

  • Casper-Lindley C, Björkman O (1998) Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynth Res 56:277–289

    CAS  Google Scholar 

  • Chevalier EM, GĂ©vaert F, CrĂ©ach A (2010) In situ photosynthetic activity and xanthophyll cycle development of undisturbed microphytobenthos in an intertidal mudflat. J Exp Mar Biol Ecol 385:44–49

    CAS  Google Scholar 

  • Chukhutsina VU, BĂ¼chel C, van Amerongen H (2013) Variations in the first steps of photosynthesis for the diatom Cyclotella meneghiniana grown under different light conditions. Biochim Biophys Acta 1027:10–18

    Google Scholar 

  • Colombo-Pallotta MF, GarcĂ­a-Mendoza E, Ladah LB (2006) Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol 42:1225–1234

    CAS  Google Scholar 

  • Consalvey MC, Paterson DM, Underwood GJC (2004) The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res 19:181–202

    Google Scholar 

  • Cruz S, Goss R, Wilhelm C, Leegood R, Horton P, Jakob T (2011) Impact of chlororespiration on non-photochemical quenching of chlorophyll fluorescence and on the regulation of the diadinoxanthin cycle in the diatom Thalassiosira pseudonana. J Exp Bot 62:509–519

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dambek M, Eilers U, Breitenbach J, Steiger S, BĂ¼chel C, Sandmann G (2012) Biosynthesis of fucoxanthin and diadinoxanthin and function of initial pathway genes in Phaeodactylum tricornutum. J Exp Bot 63:5607–5612

    CAS  PubMed Central  PubMed  Google Scholar 

  • De Martino A, Douady D, Rousseau B, Duval JC, Caron L (1997) Characterization of two light-harvesting subunits isolated from the brown alga Pelvetia canaliculata: heterogeneity of xanthophyll distribution. Photochem Photobiol 66:190–197

    Google Scholar 

  • De Martino A, Douady D, Quinet-Szely M, Rousseau B, Crepineau F, Apt K, Caron L (2000) The light-harvesting antenna of brown algae highly homologous proteins encoded by a multigene family. Eur J Biochem 267:5540–5549

    PubMed  Google Scholar 

  • De Reviers B, Rousseau F (1999) Towards a new classification of the brown algae. In: Round FE, Chapman DJ (eds) Progress in Phycological Research, Volume 13. Biopress, Bristol, pp 107–201

    Google Scholar 

  • Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Wiinter K, KrĂ¼ger A, Czygan F-C (1989) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2% O2, 0% CO2. Plant Physiol 90:887–893

    CAS  PubMed Central  PubMed  Google Scholar 

  • Demmig-Adams B, Ebbert V, Mellman DL, Mueh KE, Schaffer L, Funk C, Zarter RC, Adamska I, Jansson S, Adams WW III (2006) Modulation of PsbS and flexible vs sustained energy dissipation by light environment in different species. Physiol Plant 127:670–680

    CAS  Google Scholar 

  • Depauw FA, Rogato A, d’Alcala MR, Falciatore A (2012) Exploring the molecular basis of responses to light in marine diatoms. J Exp Bot 63:1575–1591

    CAS  PubMed  Google Scholar 

  • Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotective capacity as functional trait in planktonic algae: relationship between xanthophyll cycle and ecological characteristics in three diatoms. J Phycol 43:937–947

    CAS  Google Scholar 

  • Dimier C, Giovanni S, Ferdinando T, Brunet C (2009) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist 160:397–411

    CAS  PubMed  Google Scholar 

  • Dittami SM, Michel G, CollĂ©n J, Boyen C, Tonon T (2010) Chlorophyll-binding proteins revisited – a multigenic family of light-harvesting and stress proteins from a brown algal perspective. BMC Evol Biol 10:365–379

    CAS  PubMed Central  PubMed  Google Scholar 

  • Edwards KF, Lichtam E, Klausmeier CA (2013) Functional traits explain phytoplankton community structure and seasonal dynamics in a marine ecosystem. Ecol Lett 16:56–63

    PubMed  Google Scholar 

  • Eisenstadt D, Ohad I, Keren N, Kaplan A (2008) Changes in the photosynthetic reaction centre II in the diatom Phaeodactylum tricornutum result in non-photochemical fluorescence quenching. Environ Microbiol 10:1997–2007

    CAS  PubMed  Google Scholar 

  • Enriquez S, Borowitzka MA (2011) The use of the fluorescence signal in studies of seagrasses and macroalgae. In: Prasil O, Sugget D, Borowitzka MA (eds) Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications, Developments in Applied Phycology, Volume 4. Springer, Dordrecht, pp 187–208

    Google Scholar 

  • Enriquez MM, LaFountain AM, Budarz J, Fuciman M, Gibson GN, Frank HA (2010) Direct determination of the excited state energies of the xanthophylls diadinoxanthin and diatoxanthin from Phaeodactylum tricornutum. Chem Phys Lett 493:353–357

    CAS  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    CAS  PubMed  Google Scholar 

  • Feikema WO, Marosvölgyi MA, Lavaud J, van Gorkom HJ (2006) Cyclic electron transfer in photosystem II in the marine diatom Phaeodactylum tricornutum. Biochim Biophys Acta 1757:829–834

    CAS  Google Scholar 

  • Fork DC, Herbert SK, Malkin S (1991) Light energy distribution in the brown alga Macrocystis pyrifera (giant kelp). Plant Physiol 95:731–739

    CAS  PubMed Central  PubMed  Google Scholar 

  • Frommolt R, Werner S, Paulsen H, Goss R, Wilhelm C, Zauner S, Maier UG, Grossman AR, Bhattacharya D, Lohr M (2008) Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. Mol Biol Evol 25:2653–2667

    CAS  PubMed  Google Scholar 

  • Fujii R, Kita M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Cogdell RJ, Hashimoto H (2012) Isolation and purification of the major photosynthetic antenna, fucoxanthin-Chl a/c protein, from cultured discoid germlings of the brown alga, Cladosiphon okamuranus TOKIDA (Okinawa Mozuku). Photosynth Res 111:157–163

    CAS  PubMed  Google Scholar 

  • Fujiki T, Toda T, Kikuchi T, Taguchi S (2003) Photoprotective response of xanthophyll pigments during phytoplankton blooms in Sagami Bay, Japan. J Plankton Res 25:317–322

    CAS  Google Scholar 

  • GarcĂ­a-Mendoza E, Colombo-Pallotta MF (2007) The giant kelp Macrocystis pyrifera presents a different nonphotochemical quenching control than higher plants. New Phytol 173:526–536

    PubMed  Google Scholar 

  • GarcĂ­a-Mendoza E, Ocampo-Alvarez H, Govindjee (2011) Photoprotection in the brown alga Macrocystis pyrifera: evolutionary implications. J Photochem Photobiol B Biol 104:377–385

    Google Scholar 

  • GĂ©vaert F, CrĂ©ach A, Davoult D, Holl A-C, 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

    Google Scholar 

  • GĂ©vaert F, CrĂ©ach A, Davoult D, MignĂ© A, Levavasseur G, Arzel P, Holl A, Lemoine Y (2003) Laminaria saccharina photosynthesis measured in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Mar Ecol Prog Ser 247:43–50

    Google Scholar 

  • Giovagnetti V, Cataldo ML, Conversano F, Brunet C (2012) Growth and photophysiological responses of two picoplanktonic Minutocellus species, strains RCC967 and RCC703 (Bacillariophyceae). Eur J Phycol 47:408–420

    CAS  Google Scholar 

  • Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122

    CAS  PubMed  Google Scholar 

  • Goss R, Lohr M, Latowski D, Grzyb J, Vieler A, Wilhelm C, Strzalka K (2005) Role of hexagonal structure-forming lipids in diadinoxanthin and violaxanthin solubilization and de-epoxidation. Biochemistry 44:4028–4036

    CAS  PubMed  Google Scholar 

  • Goss R, Pinto EA, Wilhelm C, Richter M (2006a) The importance of a highly active and ΔpH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163:1008–1021

    CAS  PubMed  Google Scholar 

  • Goss R, Lepetit B, Wilhelm C (2006b) Evidence for a rebinding of antheraxanthin to the light-harvesting complex during the epoxidation reaction of the violaxanthin cycle. J Plant Physiol 163:585–590

    CAS  PubMed  Google Scholar 

  • Goss R, Latowski D, Grzyb J, Vieler A, Lohr M, Wilhelm C, Strzalka K (2007) Lipid dependence of diadinoxanthin solubilization and de-epoxidation in artificial membrane systems resembling the lipid composition of the natural thylakoid membrane. Biochim Biophys Acta 1768:67–75

    CAS  PubMed  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2006) Influence of ascorbate and pH on the activity of the diatom xanthophyll cycle-enzyme diadinoxanthin de-epoxidase. Physiol Plant 126:205–211

    CAS  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2008) A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol 49:1217–1225

    CAS  PubMed  Google Scholar 

  • Grouneva I, Jakob T, Wilhelm C, Goss R (2009) The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim Biophys Acta 1787:929–938

    CAS  PubMed  Google Scholar 

  • Gundermann K, BĂ¼chel C (2012) Factors determining the fluorescence yield of fucoxanthin-chlorophyll complexes (FCP) involved in non-photochemical quenching in diatoms. Biochim Biophys Acta 1817:1044–1052

    CAS  PubMed  Google Scholar 

  • Hager A (1967a) Untersuchungen Ă¼ber die lichtinduzierten, reversiblen Xanthophyllumwandlungen an Chlorella und Spinacia oleracea. Planta 74:148–172

    CAS  PubMed  Google Scholar 

  • Hager A (1967b) Untersuchungen Ă¼ber die RĂ¼ckreaktionen im Xanthophyll-Cyclus bei Chlorella, Spinacia und Taxus. Planta 76:138–148

    CAS  PubMed  Google Scholar 

  • Hanelt D, Wiencke C, Karsten U, Nultsch W (1997) Photoinhibition and recovery after light stress in different developmental and life history stages of Laminaria saccharina (Phaeophyta). J Phycol 33:387–395

    Google Scholar 

  • Harker M, Berkaloff C, Lemoine Y, Britton G, Young A, Duval JC, Rmiki N, 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

    Google Scholar 

  • Hashihama F, Umeda H, Hamada C, Kudoh S, Hirawake T, Satoh K, Fukuchi M, Kashino Y (2010) Light acclimation states of phytoplankton in the Southern Ocean determined using photosynthetic pigment distribution. Mar Biol 157:2263–2278

    CAS  Google Scholar 

  • Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen JMH, Sommeijer B (2004) Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85:2960–2970

    Google Scholar 

  • Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:192–193

    Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    CAS  PubMed  Google Scholar 

  • Jakob T, Goss R, Wilhelm C (1999) Activation of diadinoxanthin de-epoxidase due to a chlororespiratory proton gradient in the dark in the diatom Phaeodactylum tricornutum. Plant Biol 1:76–82

    CAS  Google Scholar 

  • Jakob T, Goss R, Wilhelm C (2001) Unusual pH-dependence of diadinoxanthin de-epoxidase activation causes chlororespiratory induced accumulation of diatoxanthin in the diatom Phaeodactylum tricornutum. J Plant Physiol 158:383–390

    CAS  Google Scholar 

  • Jesus B, Perkins RG, Consalvey MC, Brotas V, Paterson DM (2006) Effects of vertical migration by benthic microalgae on fluorescence measurements of photophysiology. Mar Ecol Prog Ser 315:55–66

    CAS  Google Scholar 

  • Jesus B, Brotas V, Ribeiro L, Mendes CR, Cartaxana P, Paterson DM (2009) Adaptations of microphytobenthos assemblages to sediment type and tidal position. Cont Shelf Res 29:1624–1634

    Google Scholar 

  • Jordan L, McMinn A, Thompson P (2010) Diurnal changes of photoadaptive pigments in microphytobenthos. J Mar Biol Assoc UK 90:1025–1032

    Google Scholar 

  • Joshi-deo J, Schmidt M, Gruber A, Weisheit W, Mittag M, Kroth PG, BĂ¼chel C (2010) Characterization of a trieric light-harvesting complex in the diatom Phaeodactylum tricornutum built of FcpA and FcpE proteins. J Exp Bot 61:3079–3087

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kalituho L, Beran KC, Jahns P (2007) The transiently generated non-photochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. Plant Physiol 143:1861–1870

    CAS  PubMed Central  PubMed  Google Scholar 

  • Katoh T, Mimuro M, Takaichi S (1989) Light-harvesting particles isolated from a brown alga, Dictyota dichtoma. A supramolecular assembly of fucoxanthin-chlorophyll-protein complexes. Biochim Biophys Acta 976:233–240

    CAS  Google Scholar 

  • Kirk JTO (2011) Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge

    Google Scholar 

  • Konotchick T, Dupont CL, Valas RE, Badger JH, Allen AE (2013) Transcriptomic analysis of metabolic function in th egiant kelp, macrocystis pyrifera, across depth and season. New Phytol 198:398–407

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kooistra WHCF, Gersonde R, Medlin LK, Mann DG (2007) The origin and the evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski PG, Knoll AH (eds) Evolution of Primary Producers in the Sea. Elsevier Academic Press, Burlington, pp 207–249

    Google Scholar 

  • Kropuenske LR, Mills MM, van Dijken GL, Bailey S, Robinson DH, Welschmeyer NA, Arrigo KR (2009) Photophysiology in two major Southern Ocean phytoplankton taxa: photoprotection in Phaeocystis antartica and Fragilaria cylindricus. Limnol Oceanogr 54:1176–1196

    CAS  Google Scholar 

  • Latowski D, Kruk J, Burda K, Skrzynecka-Jaskier M, Kostecka-Gugala A, Strzalka K (2002) Kinetics of violaxanthin de-epoxidation by violaxanthin de-epoxidase, a xanthophyll cycle enzyme, is regulated by membrane fluidity in model lipid bilayers. Eur J Biochem 269:4656–4665

    CAS  PubMed  Google Scholar 

  • Latowski D, Kuczynska P, Strzalka K (2011) Xanthophyll cycle – a mechanism protecting plants against oxidative stress. Redox Rep 16:78–90

    CAS  PubMed  Google Scholar 

  • Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Funct Plant Sci Biotech 1:267–287

    Google Scholar 

  • Lavaud J, Kroth PG (2006) In diatoms, the transthylakoid proton gradient regulates the photoprotective non-photochemical fluorescence quenching beyond its control on the xanthophyll cycle. Plant Cell Physiol 47:1010–1016

    CAS  PubMed  Google Scholar 

  • Lavaud J, Lepetit B (2013) An explanation for the inter-species variability of the photoprotective non-photochemical chlorophyll fluorescence quenching in diatoms. Biochim Biophys Acta 1827:294–302

    CAS  PubMed  Google Scholar 

  • Lavaud J, Rousseau B, van Gorkom HJ, Etienne A-L (2002a) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lavaud J, Rousseau B, Etienne A-L (2002b) In diatoms, a transthylakoidal proton gradient alone is not sufficient for non-photochemical fluorescence quenching. FEBS Lett 523:163–166

    CAS  PubMed  Google Scholar 

  • Lavaud J, van Gorkom HJ, Etienne A-L (2002c) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:49–57

    Google Scholar 

  • Lavaud J, Rousseau B, Etienne A-L (2003) Enrichment of the light-harvesting complex in diadinoxanthin and implications for the nonphotochemical quenching fluorescence quenching in diatoms. Biochemistry 42:5802–5808

    CAS  PubMed  Google Scholar 

  • Lavaud J, Rousseau B, Etienne A-L (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137

    Google Scholar 

  • Lavaud J, Strzepek R, Kroth PG (2007) Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52:1188–1194

    CAS  Google Scholar 

  • Lavaud J, Materna A, Sturm S, Vugrinec S, Kroth PG (2012) Silencing of the violaxanthin de-epoxidase gene in the diatom Phaeodactylum tricornutum reduces diatoxanthin synthesis and non-photochemical quenching. PLoS One 7:e36806

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lefebvre S, Mouget J-L, Lavaud J (2011) Duration of rapid light curves for determining in situ the photosynthetis of microphytobenthos biofilms. Aquat Bot 95:1–8

    CAS  Google Scholar 

  • Lepetit B, Volke D, Szabo M, Hoffmann R, Garab G, Wilhelm C, Goss R (2007) Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. Biochemistry 46:9813–9822

    CAS  PubMed  Google Scholar 

  • Lepetit B, Volke D, Gilbert M, Wilhelm C, Goss R (2010) Evidence for the existence of one antenna-associated, lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol 154:1905–1920

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lepetit B, Goss R, Jakob T, Wilhelm C (2012) Molecular dynamics of the diatom thylakoid membrane under different light conditions. Photosynth Res 111:245–257

    CAS  PubMed  Google Scholar 

  • Lepetit B, Sturm S, Rogato A, Gruber A, Sachse M, Falciatore A, Kroth PG, Lavaud J (2013) High light acclimation in the secondary plastids containing diatom Phaeodactylum tricornutum is triggered by the redox state of the plastoquinone pool. Plant Physiol 161:863–865

    Google Scholar 

  • Li Z, Wakao S, Fisher BB, Niyogi K (2009) Sensing and responding to excess light. Ann Rev Plant Biol 60:239–260

    CAS  Google Scholar 

  • Lohr M (2011) Carotenoid metabolism in phytoplankton. In: Roy S, Llewellyn CA, Skarstad E, Johnsen G (eds) Phytoplankton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography. Cambridge University Press, Cambridge, pp 113–161

    Google Scholar 

  • Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96:8784–8789

    CAS  PubMed Central  PubMed  Google Scholar 

  • MacIntyre HL, Kana TM, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5:12–17

    CAS  PubMed  Google Scholar 

  • Materna A, Sturm S, Kroth PG, Lavaud J (2009) First induced plastid genome mutations in an alga with secondary plastids: psbA mutations in the diatom Phaeodactylum tricornutum (Bacillariophyceae) reveal consequences on the regulation of photosynthesis. J Phycol 45:838–846

    CAS  Google Scholar 

  • McKew BA, Davey P, Finch SJ, Hopkins J, Lefebvre SC, Metodiev MV, Oxborough K, Raines CA, Lawson T, Geider RJ (2013) The trade-off between the light-harvesting and photoprotective functions of fucoxanthin-chlorophyll proteins dominates light acclimation in Emiliana huxleyi (clone CCMP 1516). New Phytol 200:74–85.

    Google Scholar 

  • Mewes H, Richter M (2002) Supplementary ultraviolet-B radiation induces a rapid reversal of the diadinoxanthin cycle in the strong light-exposed diatom Phaeodactylum tricornutum. Plant Physiol 130:1527–1535

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meyer AA, Tackx M, Daro N (2000) Xanthophyll cycling in Phaeocystis globosa and Thalassiosira sp.: a possible mechanism for species succession. J Sea Res 43:373–384

    CAS  Google Scholar 

  • Mills MM, Kropuenske LR, van Dijken GL, Alderkamp A-C, Berg GM, Robinson DH, Welschmeyer NA, Arrigo KR (2010) Photophysiology in two Southern ocean phytoplankton taxa: photosynthesis of Phaeocystis antarctica (Prymnesiophyceae) and Fragilaria cylindrus (Bacillariophyceae) under simulated mixed-layer irradiance. J Phycol 46:1114–1127

    CAS  Google Scholar 

  • Miloslavina Y, Grouneva I, Lambrev PH, Lepetit B, Goss R, Wilhelm C, Holzwarth AR (2009) Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim Biophys Acta 1787:1189–1197

    CAS  PubMed  Google Scholar 

  • Mouget J-L, Perkins RG, Consalvey M, Lefebvre S (2008) Migration or photoacclimation to prevent high irradiance and UV-B damage in marine microphytobenthic communities. Aquat Microb Ecol 52:223–232

    Google Scholar 

  • Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726

    CAS  PubMed  Google Scholar 

  • Nitschke U, Connan S, Stengel DB (2012) Chlorophyll a fluorescence responses of temperate Phaeophyceae under submersion and emersion regimes: a comparison of rapid and steady-state light curves. Photosynth Res 114:29–42

    CAS  PubMed  Google Scholar 

  • Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314

    CAS  PubMed  Google Scholar 

  • Ocampo-Alvarez H, GarcĂ­a-Mendoza E, Govindjee (2013) Antagonistic effect between violaxanthin and de-epoxidated pigments in nonphotochemical quenching induction in the qE deficient brown alga Macrocystis pyrifera. Biochim Biophys Acta 1827:427–437

    CAS  PubMed  Google Scholar 

  • Owens TG (1986) Light-harvesting function in the diatom Phaeodactylum tricornutum II. Distribution of excitation energy between the photosystems. Plant Physiol 80:739–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • Passaquet C, Thomas JC, Caron L, Hauswith N, Puel F, Berkaloff C (1991) Light-harvesting complexes of brown algae. Biochemical characterization and immunological relationships. FEBS Lett 280:21–26

    CAS  PubMed  Google Scholar 

  • Perkins RG, Mouget JL, Lefebvre S, Lavaud J (2006) Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic diatoms. Mar Biol 149:703–712

    Google Scholar 

  • Perkins R, Lavaud J, SerĂ´dio J, Mouget J-L, Cartaxana P, Rosa P, BarrillĂ© L, Brotas V, Jesus B (2010) Vertical cell movement is the primary response of intertidal benthic biofilms to increasing light dose. Mar Ecol Prog Ser 416:93–103

    CAS  Google Scholar 

  • Perkins R, Kromkamp JC, SerĂ´dio J, Lavaud J, Jesus B, Mouget J-L, Lefebvre S, Forster RM (2011) The application of variable chlorophyll fluorescence to microphytobenthic biofilms. In: Prasil O, Sugger D, Borowitzka MA (eds) Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications, Developments in Applied Phycology, Volume 4. Springer, Dordrecht, pp 237–276

    Google Scholar 

  • Petrou K, Doblin MA, Ralph PJ (2011) Heterogeneity in the photoprotective capacity of three Antarctic diatoms during short-term changes in salinity and temperature. Mar Biol 158:1029–1041

    Google Scholar 

  • Philips N, Burrowes R, Rousseau F, de Reviers B, Saunders GW (2008) Resolving evolutionary relationships among the brown algae using chloroplast and nuclear genes. J Phycol 44:394–405

    Google Scholar 

  • Poulson ME, McNeil AJ, Donahue RA (2011) Photosynthetic response of Nereocystis luetkeana (Phaeophyta) to high light. Phycol Res 59:156–165

    Google Scholar 

  • Pyszniak AM, Gibbs SP (1992) Immunocytochemical localization of photosystem I and the fucoxanthin-chlorophyll a/c light-harvesting complex in the diatom Phaeodactylum tricornutum. Protoplasma 166:208–217

    CAS  Google Scholar 

  • Rodrigues MA, Santos CPD, Young AJ, Strbac D, Hall DO (2002) A smaller and impaired xanthophyll cycle makes the deep sea algae Laminaria abyssalis (Phaeophyceae) highly sensitive to daylight when compared with shallow water Laminaria digitata. J Phycol 38:939–947

    Google Scholar 

  • Ruban AV, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne A-L (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175

    CAS  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181

    CAS  PubMed  Google Scholar 

  • Saga G, Giorgetti A, Fufezan C, Giacometti GM, Bassi R, Morosinotto T (2010) Mutation analysis of violaxanthin de-epoxidase indentifies substrate-binding sites and residues involved in catalysis. J Biol Chem 285:23763–23770

    CAS  PubMed Central  PubMed  Google Scholar 

  • Salleh S, McMinn A (2011) The effects of temperature on the photosynthetic parameters and recovery of two temperate benthic microalgae, Amphora cf.coffeaeformis and Cocconeis cf. sublittoralis (Bacillariophyceae). J Phycol 47:1413–1424

    Google Scholar 

  • Schaller S, Latowski D, Jemiola-Rzeminska M, Wilhelm C, Strzalka K, Goss R (2010) The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim Biophys Acta 1797:414–424

    CAS  PubMed  Google Scholar 

  • Schaller S, Wilhelm C, Strzalka K, Goss R (2012) Investigating the interaction between the violaxanthin cycle enzyme zeaxanthin epoxidase and the thylakoid membrane. J Photochem Photobiol B 114:119–125

    CAS  PubMed  Google Scholar 

  • Schellenberger Costa B, Sachse M, Jungandreas A, Rio Bartulos C, Gruber A, Jakob T, Kroth PG, Wilhelm C (2013) Aureochrome 1a is involved in the photoacclimation of the diatom. Phaeodactylum tricornutum. PLoS ONE 8:e74451

    Google Scholar 

  • Schofield O, Evens TJ, Mille DF (1998) Photosystem II quantum yields and xanthophyll-cycle pigments of the macroalga Sargassum natans (Phaeophyceae): responses under natural sunlight. J Phycol 34:104–112

    CAS  Google Scholar 

  • Schumann A, Goss R, Jakob T, Wilhelm C (2007) Investigation of the quenching efficiency of diatoxanthin in cells of Phaeodactylum tricornutum (Bacillariophyceae) with different pool sizes of xanthophyll cycle pigments. Phycologia 46:113–117

    Google Scholar 

  • SerĂ´dio J, Lavaud J (2011) A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res 108:61–76

    PubMed  Google Scholar 

  • SerĂ´dio J, Cruz S, Vieira S, Brotas V (2005) Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos. J Exp Mar Biol Ecol 326:157–169

    Google Scholar 

  • SerĂ´dio J, Vieira S, Cruz S (2008) Photosynthetic activity, photoprotection and photoinhibition in intertidal microphytobenthos as studied in situ using variable chlorophyll fluorescence. Cont Shelf Res 28:1363–1375

    Google Scholar 

  • SerĂ´dio J, EzĂ©quiel J, Barnett A, Mouget J-L, MĂ©lĂ©der V, Laviale M, Lavaud J (2012) Efficiency of photoprotection in microphytobenthos: role of vertical migration and the xanthophyll cycle against photoinhbition. Aquat Microb Ecol 67:161–175

    Google Scholar 

  • Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431:689–692

    CAS  PubMed  Google Scholar 

  • Su W, Jakob T, Wilhelm C (2012) The impact of nonphotochemical quanching of fluorescence on the photon balance in diatoms under dynamic light conditions. J Phycol 48:336–346

    CAS  Google Scholar 

  • Szabo M, Lepetit B, Goss R, Wilhelm C, Mustardy L, Garab G (2008) Structurally flexible macro-organization of the pigment-protein complexes of the diatom Phaeodactylum tricornutum. Photosynth Res 95:237–245

    CAS  PubMed  Google Scholar 

  • Tozzi S, Schofield O, Falkowski PG (2004) Historical climate change and ocean turbulence as selective agents for two key phytoplankton functional groups. Mar Ecol Prog Ser 274:123–132

    Google Scholar 

  • Tuji A (2000) The effect of irradiance on the growth of different forms of freshwater diatoms: implications for succession in attached diatom communities. J Phycol 36:659–661

    Google Scholar 

  • Uhrmacher S, Hanelt D, Nultsch W (1995) Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma. Mar Biol 123:159–165

    CAS  Google Scholar 

  • Underwood GJC, Kromkamp J (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Adv Ecol Res 29:93–153

    CAS  Google Scholar 

  • Underwood GJC, Perkins RG, Consalvey MC, Hanlon ARM, Oxborough K, Baker NR, Paterson DM (2005) Patterns in microphytobenthic primary productivity: species-specific variation in migratory rhythms and photosynthetic efficiency in mixed-species biofilms. Limnol Oceanogr 50:755–767

    Google Scholar 

  • Ursi S, PedersĂ©n M, Plastino E, Snoeijs P (2003) Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Mar Biol 142:997–1007

    CAS  Google Scholar 

  • van de Poll WH, Alderkamp A-C, Janknegt PJ, Roggeveld J, Buma AGJ (2006) Photoacclimation modulates excessive photosynthetically active and ultraviolet radiation effects in a temperate and an Antarctic marine diatom. Limnol Oceanogr 51:1239–1248

    Google Scholar 

  • van de Poll WH, Lagunas M, de Vries T, Visser RJW, Buma AGJ (2011) Non-photochemical quenching of chlorophyll fluorescence and xanthophyll cycle responses after excess PAR and UVR in Chaetoceros brevis, Phaeocystis antarctica and coastal Antarctic phytoplankton. Mar Ecol Prog Ser 426:119–131

    Google Scholar 

  • van Leeuwe MA, van Sikkelerus B, Gieskes WWC, Stefels J (2005) Taxon-specific differences in photoacclimation to fluctuating irradiance in an Antarctic diatom and a green flagellate. Mar Ecol Prog Ser 288:9–19

    Google Scholar 

  • van Leeuwe MA, Brotas V, Consalvey M, Forster RM, Gillespie D, Jesus B, Roggeveld J, Gieskes WWC (2009) Photacclimation in microphytobenthos and the role of the xanthophyll pigments. Eur J Phycol 43:123–132

    Google Scholar 

  • Veith T, Brauns J, Weisheit W, Mittag M, BĂ¼chel C (2009) Identification of a specific fucoxanthin-chlorophyll protein in the light-harvesting complex of photosystem I in the diatom Cyclotella meneghiniana. Biochim Biophys Acta 1787:905–915

    CAS  PubMed  Google Scholar 

  • Wagner H, Jakob T, Wilhelm C (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol 169:95–108

    CAS  PubMed  Google Scholar 

  • Waring J, Underwoord GJC, Baker NR (2006) Impact of elevated UV-B radiation on photosynthetic electron transport, primary productivity and carbon allocation in estuarine epipelic diatoms. Plant Cell Environ 29:521–534

    CAS  PubMed  Google Scholar 

  • Waring J, Baker NR, Underwoord GJC (2007) Responses of estuarine intertidal microphytobenthic algal assemblages to enhanced ultraviolet B radiation. Glob Chang Biol 13:1398–1413

    Google Scholar 

  • Wiencke C, Bischof K (eds) (2012) Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization, Volume 510. Springer, Berlin, p 219

    Google Scholar 

  • Wilhelm C, BĂ¼chel C, Fisahn J, Goss R, Jakob T, LaRoche J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG (2006) The regulation of photosynthetic carbon and nutrient assimilation in diatoms is significantly different from green algae, a putative consequence of secondary endosymbiosis. Protist 157:91–124

    CAS  PubMed  Google Scholar 

  • Wu H, Roy S, Alami M, Green BR, Campbell DA (2012) Photosystem II photoinactivation, repair, and protection in marine centric diatoms. Plant Physiol 160:464–476

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto H, Nakayama T, Chichester C (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97:168–173

    CAS  PubMed  Google Scholar 

  • Zhu S-H, Green BR (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 1797:1449–1457

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

JL thanks the Centre National de la Recherche Scientifique (CNRS), the UniversitĂ© de La Rochelle (ULR), the Contrat Plan Etat RĂ©gion (CPER) ‘Littoral’, the RĂ©gion Poitou-Charentes (CG17), the Deutsche Forschungsgemeinschaft (DFG, grant LA2368/2-1), the Deutsche Akademische Austauschdienst (DAAD), and Egide/Campus France (grants 27377TB and 28992UA) for their financial support. RG thanks the DFG (grants Go818/6-1, Go818/7-1) for its financial support. The two authors thank B. Lepetit for his help building and drawing the model of Fig. 20.2. JL dedicates this work to his mentors Pr. J.-C. Duval and Dr. A.-L. Etienne.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johann Lavaud .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Lavaud, J., Goss, R. (2014). The Peculiar Features of Non-Photochemical Fluorescence Quenching in Diatoms and Brown Algae. In: Demmig-Adams, B., Garab, G., Adams III, W., Govindjee, . (eds) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration, vol 40. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9032-1_20

Download citation

Publish with us

Policies and ethics