Efficiency of photoprotection in microphytobenthos: Role of vertical migration and the xanthophyll cycle against photoinhibition

Aquatic Microbial Ecology

Volumn 67, Issue 2, 2012, Pages 161-175

  Serôdio, João ^a,b   Ezequiel, João ^a   Barnett, Alexandre ^b   Mouget, Jean Luc ^c   Meĺéder, Vona ^b,d   Laviale, Martin ^a,d   Lavaud, Johann ^b  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITÉ DE LA ROCHELLE   (France)

^c UNIVERSITÉ DU MAINE   (France)

^d UNIVERSITÉ DE NANTES   (France)

Author keywords

Chlorophyll fluorescence; Diatoms; Microphytobenthos; Non photochemical quenching; Photoinhibition; Photoprotection; Vertical migration; Xanthophyll cycle

Indexed keywords

BACILLARIOPHYTA;

EID: 84872475298     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01591     Document Type: Article

References (73)

1. Admiraal W (1984) The ecology of estuarine sedimentinhabiting diatoms. Prog Phycol Res 3:269-322
2. Ahn TK, Avenson TJ, Peers G, Li Z and others (2009) Investigating energy partitioning during photosynthesis using an expanded quantum yield convention. Chem Phys 357: 151-158
3. Behrenfeld MJ, Prasil O, Babin M, Bruyant F (2004) In search of a physiological basis for covariations in lightlimited and light-saturated photosynthesis. J Phycol 40: 4-25 (Pubitemid 38241632)
4. Blanchard GF, Cariou-Le Gall V (1994) Photosynthetic characteristics of microphytobenthos in MarennesOléron Bay, France: preliminary results. J Exp Mar Biol Ecol 182:1-14
5. Blanchard GF, Guarini JM, Gros P, Richard P (1997) Seasonal effect on the relationship between the photosynthetic capacity of intertidal microphytobenthos and temperature. J Phycol 33:723-728 (Pubitemid 27471699)
6. Blanchard GF, Guarini JM, Dang C, Richard P (2004) Characterizing and quantifying photoinhibition in intertidal microphytobenthos. J Phycol 40:692-696 (Pubitemid 39059708)
7. Brotas V, Risgaard-Petersen N, Ottossen L, Serôdio J, Ribeiro L, Dalsgaard T (2003) In situ measurement of photosynthetic activity and respiration of intertidal benthic microalgal communities undergoing vertical migration. Ophelia 57:13-26 (Pubitemid 36715003)
8. 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
9. Cartaxana P, Serôdio J (2008) Inhibiting diatom motility: a new tool for the study of the photophysiology of intertidal microphytobenthic biofilms. Limnol Oceanogr Methods 6:466-476
10. Cartaxana P, Brotas V, Serôdio J (2008) Effects of two motility inhibitors on the photosynthetic activity of the diatoms Cylindrotheca closterium and Pleurosigma angulation. Diatom Res 23:65-74 (Pubitemid 351676259)
11. Cartaxana P, Ruivo M, Hubas C, Davidson I, Serôdio J, Jesus B (2011) Physiological versus behavioural photoprotection in intertidal epipelic and epipsamic benthic diatom communities. J Exp Mar Biol Ecol 405:120-127
12. Chevalier EM, Gévaert F, Créach A (2010) In situ photosynthetic activity and xanthophylls cycle development of undisturbed microphytobenthos in an intertidal mudflat. J Exp Mar Biol Ecol 385:44-49
13. Coelho H, Vieira S, Serôdio J (2009) Effects of desiccation on the photosynthetic activity of intertidal microphytobenthos biofilms as studied by optical methods. J Exp Mar Biol Ecol 381:98-104
14. Coelho H, Vieira S, Serôdio J (2011) Endogenous versus environmental control of vertical migration by intertidal benthic microalgae. Eur J Phycol 46:271-281
15. Consalvey M, Paterson DM, Underwood GJC (2004) The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res 19:181-202 (Pubitemid 39526842)
16. 2 limitation in microphytobenthos in highly productive sandy sediments. Limnol Oceanogr 51:1594-1601
17. Cruz S, Serôdio J (2008) Relationship of rapid light curves of variable fluorescence to photoacclimation and non-photochemical quenching in a benthic diatom. Aquat Bot 88: 256-264
18. 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
19. Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Modell 42: 199-215 (Pubitemid 19324509)
20. Forster RM, Kromkamp JC (2004) Modelling the effects of chlorophyll fluorescence from subsurface layers on photosynthetic efficiency measurements in microphytobenthic algae. Mar Ecol Prog Ser 284:9-22 (Pubitemid 40118202)
21. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87-92
22. Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106: 103-122
23. Goss R, Pinto AE, Wilhelm C, Richter M (2006) The importance of a highly active and ApH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin containing algae. J Plant Physiol 163: 1008-1021 (Pubitemid 44333134)
24. Guadagno CR, Virzo De Santo A, D'Ambrosio N (2010) A revised energy partitioning approach to assess the yields of non-photochemical quenching components. Biochim Biophys Acta 1797:525-530
25. Hay SI, Maitland TC, Paterson DM (1993) The speed of diatom migration through natural and artificial substrata. Diatom Res 8:371-384
26. Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729-739
27. Herlory O, Guarini JM, Richard P, Blanchard GF (2004) Microstructure of microphytobenthic biofilm and its spatio-temporal dynamics in an intertidal mudflat (Aiguillon Bay, France). Mar Ecol Prog Ser 282:33-44 (Pubitemid 39661285)
28. Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. 4. Resolution of non-photochemical quenching. Biochim Biophys Acta 932:107-115
29. 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 (Pubitemid 32235398)
30. Jesus B, Perkins RG, Consalvey M, Brotas V, Paterson DM (2006) Effects of vertical migrations by benthic microalgae on fluorescence measurements of photophysiology. Mar Ecol Prog Ser 315:55-66 (Pubitemid 44073849)
31. Jordan L, McMinn A, Thompson P (2010) Diurnal changes of photoadaptive pigments in microphytobenthos. J Mar Biol Assoc UK 90:1025-1032
32. Kromkamp J, Barranguet C, Peene J (1998) Determination of microphytobenthos PSII quantum efficiency and photosynthetic activity by means of variable chlorophyll fluorescence. Mar Ecol Prog Ser 162:45-55 (Pubitemid 28140038)
33. Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Funct Plant Sei Biotechnol 1:267-287
34. Lavaud J, Rousseau B, Etienne AL (2002a) In diatoms, a transthylakoidal proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 523:163-166 (Pubitemid 34786079)
35. Lavaud J, Gorkom HJV, Etienne AL (2002b) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:51-59 (Pubitemid 35399812)
36. Lavaud J, Rousseau B, Etienne AL (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40: 130-137 (Pubitemid 38241645)
37. Maclntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17-38 (Pubitemid 34196829)
38. Méléder V, Rincé Y, Barillé L, Gaudin P, Rosa P (2007) Spatio-temporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf Bay, France). J Phycol 43: 1177-1190 (Pubitemid 350221968)
39. Migné A, Spilmont N, Davoult D (2004) In situ measurements of benthic primary production during emersion: seasonal variations and annual production in the Bay of Somme (eastern English Channel, France). Cont Shelf Res 24:1437-1449 (Pubitemid 39115887)
40. Miles A, Sundbäck K (2000) Diel variation in microphytobenthic productivity in areas of different tidal amplitude. Mar Ecol Prog Ser 205:11-22
41. Mouget JL, Perkins R, 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
42. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558-1566 (Pubitemid 32375740)
43. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742-749 (Pubitemid 44160685)
44. Olaizola M, Yamamoto HY (1994) Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). J Phycol 30:606-612
45. Owens TG (1986) Light-harvesting function in the diatom Phaeodactylum tricornutum II. Distribution of excitation energy between the photosystems. Plant Physiol 80: 732-738
46. Oxborough K, Hanlon ARM, Underwood GJC, Baker NR (2000) In vivo estimation of the photosystem II photochemical efficiency of individual microphytobenthic cells using high-resolution imaging of chlorophyll a fluorescence. Limnol Oceanogr 45:1420-1425
47. 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 (Pubitemid 43989362)
48. Perkins RG, Kromkamp J, Serôdio J, Lavaud J and others (2010a) The application oí variable chlorophyll fluorescence to microphytobenthic biofilms. In: Sugget D, Prasil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications, Series: developments in applied phycology, Vol 4. Springer, Dordrecht, p 237-276
49. Perkins RG, Lavaud J, Serôdio J, Mouget JL and others (2010b) Vertical cell movement is the primary response of intertidal benthic biofilms to increasing light dose. Mar Ecol Prog Ser 416:93-103
50. Ribeiro L (2010) Intertidal benthic diatoms of the Tagus estuary: taxonomic composition and spatial-temporal variation. PhD thesis, University of Lisbon
51. Rijstenbil JW (2005) UV- and salinity-induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion. Mar Biol 147:1063-1073
52. Ritchie RJ (2008) Fitting light saturation curves measured using modulated fluorometry. Photosynth Res 96: 201-215
53. N). Photosynth Res 105:101-113
54. Roncarati F, Rijstenbil JW, Pistocchi R (2008) Photosynthetic performance, oxidative damage and antioxidants in Cylindrotheca closterium in response to high irradiance, UVB radiation and salinity. Mar Biol 153:965-973
55. Ruban AV, Horton (1995) An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated chloroplasts and leaves of spinach. Plant Physiol 108:721-726
56. 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
57. Schumann A, Goss R, Jakob T, Wilhelm C (2007) Investigations on the quenching efficiency of diatoxanthin in cells of Phaeodactylum tricornutum (Bacillariophyceae) with different pool sizes of xanthophyll cycle pigments. Phycologia 46:113-117 (Pubitemid 46106729)
58. Serôdio J (2004) Analysis of variable chlorophyll fluorescence in microphytobenthos assemblages: implications of the use of depth-integrated measurements. Aquat Microb Ecol 36:137-152
59. Serôdio J, Catarino F (1999) Fortnightly light and temperature variability on estuarine intertidal sediments and implications for microphytobenthos primary productivity. Aquat Ecol 33:235-241 (Pubitemid 30213350)
60. Serôdio J, Lavaud J (2011) A model for describing the light response of the non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 108:61-76
61. Serôdio 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 (Pubitemid 41654829)
62. Serôdio J, Vieira S, Cruz S, Coelho H (2006) Rapid lightresponse curves of chlorophyll fluorescence in microalgae: relationship to steady-state light curves and nonphotochemical quenching in benthic diatom-dominated assemblages. Photosynth Res 90:29-43 (Pubitemid 46112679)
63. Serôdio 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
64. Underwood GJC (2002) Adaptations of tropical marine microphytobenthic assemblages along a gradient of light and nutrient availability in Suva Lagoon, Fiji. Eur J Phycol 37:449-462
65. Underwood GJC, Kromkamp J (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Adv Ecol Res 29:93-153
66. Underwood GJC, Nilsson C, Sundbäck K, Wulff A (1999) Short-term effects of UVB radiation on chlorophyll fluorescence, biomass, pigments, and carbohydrate fractions in a benthic diatom mat. J Phycol 35:656-666 (Pubitemid 29407467)
67. 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 (Pubitemid 40764363)
68. Van Leeuwe MA, Brotas V, Consalvey M, Forster RM and others (2008) Photoacclimation in microphytobenthos and the role of xanthophyll pigments. Eur J Phycol 43: 123-132 (Pubitemid 351883044)
69. Walters RG, Horton P (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121-133
70. Waring J, Baker NR, Underwood GJC (2007) Responses of estuarine intertidal microphytobenthic algal assemblages to enhanced ultraviolet B radiation. Glob Change Biol 13:1398-1413 (Pubitemid 47082273)
71. Waring J, Klenell M, Bechtold U, Underwood GJC, Baker NR (2010) Light-induced responses of oxygen photoreduction, reactive oxygen species production and scavenging in two diatom species. J Phycol 46:1206-1217
72. Wu H, Cockshutt AM, McCarthy A, Campbell DA (2011) Distinctive photosystem II photoinactivation and protein dynamics in marine diatoms. Plant Physiol 156: 2184-2195
73. Wulff A, Roleda MY, Zacher K, Wiencke C (2008) UV radiation effects on pigments, photosynthetic efficiency and DNA of a semi-natural Antarctic marine benthic diatom community. Aquat Biol 3:167-177