Continuous monitoring of in vivo chlorophyll a fluorescence in ulva rigida (Chlorophyta) submitted to different CO2, nutrient and temperature regimes

Aquatic Biology

Volumn 22, Issue , 2014, Pages 195-212

  Figueroa, F L ^a   Conde Alvarez R ^a   Bonomi Barufi, J ^b   Celis Pla P S ^a   Flores, P ^a   Malta, E J ^c   Stengel, D B ^d   Meyerhoff, O ^e   Perez Ruzafa A ^f  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^c IFAPA CENTRO EL TORUÑO   (Spain)

^d NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^e Heinz Walz GmbH   (Germany)

^f UNIVERSITY OF MURCIA   (Spain)

Author keywords

Climate change; In vivo chlorophyll fluorescence; Monitoring PAM; Nitrate; Ocean acidification; Temperature; Ulva rigida

Indexed keywords

CHLOROPHYTA; ULVA RIGIDA;

EID: 84926294138     PISSN: 18647782     EISSN: 18647790     Source Type: Journal    
DOI: 10.3354/ab00593     Document Type: Article

References (74)

1. Axelsson L, Ryberg H, Beer S (1995) Two modes of bicar - bonate utilization in the marine green macroalga Ulva lactuca. Plant Cell Environ 18: 439-445.
2. Azuara MP, Aparicio PJ (1985) Spectral dependence of photoregulation of inorganic nitrogen metabolism in Chlamydomonas reinhardii. Plant Physiol 77: 95-98.
3. Barták M, Vácziu P, Hákjek J (2012) Photosynthetic activity in three vascular species of Spitbergen vegetation during summer season in response to microclimate. Pol Polar Res 33: 443-462.
4. Beardall J, Quigg A, Raven JA (2003) Oxygen consumption: photorespiration and chlorespiration. In: Larkum AW, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer Academic Publishers, Dordrecht, p 157-181.
5. Beer S, Larsson C, Poryan O, Axelsson L (2000) Photo - synthetic rates of Ulva (Chlorophyta) measured by pulse amplitude modulated (PAM) fluorometer. Eur J Phycol 35: 69-74.
6. Brewer PG (1997) Ocean chemistry of the fossil fuel CO2 signal: the haline signal of ‘business as usual’. Geophys Res Lett 24: 1367-1369.
7. Cabello-Pasini A, Figueroa FL (2005) Effect of nitrate concentration on the relation between photosynthetic oxygen evolution and electron transport rate in Ulva rigida (Chlorophyta). J Phycol 41: 1169-1177.
8. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425: 365.
9. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1: 169-192.
10. Enríquez S, Borowitzka MA (2011) The use of the fluorescence signal in studies of seagrasses and macroalgae. In: Suggett DJ, Borowitzka M, Ondrej P (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Developments in applied phycology, Vol 4. Springer Science+Business Media, Dordrecht, p 187-208.
11. Figueroa FL, Viñegla B (2001) Effects of solar UV radiation on photosynthesis and enzyme activities (carbonic anhydrase and nitrate reductase) in marine macroalgae from southern Spain. Rev Chil Hist Nat 74: 237-249.
12. Figueroa FL, Salles S, Aguilera J, Jiménez C and others (1997) Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar Ecol Prog Ser 151: 81-90.
13. Figueroa FL, Conde-Álvarez R, Gómez I (2003) Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth Res 75: 259-275.
14. Figueroa FL, Martínez B, Israel A, Neori A and others (2009) Acclimation of Red Sea macroalgae to solar radiation: photosynthesis and thallus absorptance. Aquat Biol 7: 159-172.
15. Figueroa FL, Jerez C, Korbee N (2013) Use of in vivo chlo - rophyll fluorescence to estimate photosynthetic activity and biomass productivity in microalgae grown in different culture systems. Lat Am J Aquatic Res 41: 801-819.
16. Figueroa FL, Bonomi Barufi J, Malta EJ, Conde-Álvarez R and others (2014) Short-term effects of increasing CO2 , nitrate and temperature on three Mediterranean macroalgae: biochemical composition. Aquat Biol 22:177–193.
17. Flexas J, Briantais JM, Cerovic Z, Medrano H, Moya I (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new re - mote sensing system. Remote Sens Environ 73: 283-297.
18. Foyer CH, Neukermans J, Quavel G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63: 1637-1661.
19. Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993) Calcification in the articulated coralline alga Co - ral lina pilulifera with special reference to the effect of elevated CO2 concentration. Mar Biol 117: 129-132.
20. Ghassemian M, Lutes J, Tepperman JM, Chang HS and others (2006) Integrative analysis of transcript and meta - bolite profiling data sets to evaluate the regulation of biochemical pathways during photomorphogenesis. Arch Biochem Biophys 448: 45-59.
21. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131.
22. Gordillo FJL, Niell FX, Figueroa FL (2001) Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213: 64-70.
23. Gordillo FJL, Figueroa FL, Niell FX (2003) Photon and carbon use efficiency in Ulva rigida at different CO2 and N levels. Planta 218: 315-322.
24. A Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22: 131-160.
25. 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.
26. Henley WJ, Levavasseur G, Franklin LA, Lindley ST, Ramus J, Osmond CB (1991) Diurnal responses of photosynthesis and fluorescence in Ulva rotundata acclimated to sun and shade in outdoor culture. Mar Ecol Prog Ser 75: 19-28.
27. Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17: 2488-2497.
28. Huovinen P, Matos J, Sousa-Pinto I, Figueroa FL (2006) The role of ammonium in photoprotection against high irradiance in the red alga Grateloupia lanceola. Aquat Bot 84: 308-316.
29. Hurd C, Hepburn C, Currie K, Raven J, Hunter A (2009) Testing the effects of ocean acidification on algal meta - bolism: considerations for experimental designs. J Phycol 45: 1236-1251.
30. Ihnken S, Eggert A, Beardall J (2010) Exposure times in rapid light curves affect photosynthetic parameters in algae. Aquat Bot 93: 185-194.
31. Johnsen G, Sakshaug E (2007) Biooptical characteristics of PSII and PSI in 33 species (13 pigment groups) of marine phytoplankton, and the relevance for pulse-amplitudemodulated and fast-repetition-rate fluorometry. J Phycol 43: 1236-1251.
32. Korbee N, Figueroa FL, Aguilera J (2005) Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photochem Photobiol B 80: 71-78.
33. Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. II. Interpretation of fluorescence signals. Photosynth Res 5: 139-157.
34. Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, New York, NY.
35. Longstaff BJ, Kildea T, Runcie JW, Cheshire A and others (2002) An in situ study of photosynthetic oxygen evolution exchange and electro transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynth Res 74: 281-293.
36. López-Figueroa F, Rüdiger W (1991) Stimulation of nitrate net uptake and reduction by red and blue light and the reversion by far-red light in the green alga Ulva rigida. J Phycol 27: 389-394.
37. Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coor - dinated regulation of genome expression and cellular pathways. Plant Cell 13: 2589-2607.
38. Maheshwari V, Dwivedi U, Bhardwaj R, Mishra M (1992) Mechanism of reductive photoactivation of enzyme of C4 pathway. J Biosci 17: 183-192.
39. Marek MV, Kalina J, Matouskova M (1995) Response of photosynthetic carbon assimilation of Norway Spruce exposed to long-term elevation of CO2 concentration. Photosynthetica 31: 209-220.
40. Martin S, Gattuso JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15: 2089-2100.
41. Martínez B, Arenas F, Rubal M, Burgués S and others (2012) Physical factors driving intertidal macroalgae distribution: physiological stress of a dominant fucoid at its southern limit. Oecologia 170: 341-353.
42. McMinn A, Ryan K, Gademann R (2003) Diurnal changes of Antarctic fast ice algal communities determined by pulse amplitude modulation fluorometry. Mar Biol 143: 359-367.
43. Meehl GA, Stocker TF, Collins WD, Friedlingstein P and others (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z and others (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 749-845.
44. Mercado JM (2008) Effects of the acidification on photosynthesis and growth of marine algae: a reappraisal of the laboratory data and their applicability to the natural habitats. In: Hagen KN (ed) Algae: nutrition, pollution control and energy sources. Nova Science Publishers, New York, NY, p 1-20.
45. Mercado JM, Cortés D, Ramírez T, Gómez F (2012) Decadal weakening of the wind-induced upwelling reduces the impact of nutrient pollution in the Bay of Málaga (western Mediterranean Sea). Hydrobiologia 680: 91-107.
46. Mercado JM, Gordillo FJL, Figueroa FL, Niell FX (1998) External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae. J Exp Mar Biol Ecol 221: 209-220.
47. Nishihara GN, Terada R, Noro T (2005) Effect of temperature and irradiance on the uptake of ammonium and nitrate by Laurencia brongniartii (Rhodophya, Ceramiales). J Appl Phycol 17: 371-377.
48. Nishiyama Y, Allarkhverdiev 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.
49. Nitschke U, Connan S, Stengel D (2012) Chlorophyll a fluorescence responses of temperate Phaeophyceae under submersion and emersion regimes: a comparison of a rapid and steady-state light curves. Photosynth Res 114: 29-42.
50. Olischläger M, Bartsch I, Gutow L, Wiencke C (2013) Effects of ocean acidification on growth and physiology of Ulva lactuca (Chlorophyla) in a rockpool-scenario. Phycol Res 61: 180-190.
51. Orr JC, Fabry VF, Aumont O, Bopp L and others (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.
52. Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans. II. CO2 assimilation and metabolite contents. Plant Physiol 112: 1253-1260.
53. Pelejero C, Calvo E, Hoegh-Guldberg O (2011) Paleoperspectives on ocean acidification. Trends Ecol Evol 25: 332-344.
54. Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53: 523-550.
55. Pérez-Lloréns JL, Vergara J, Pino R, Hernández I, Peralta G, Niell FX (1996) The effect of photoacclimation on the photosynthetic physiology of Ulva curvata and Ulva ro - tundata (Ulvales, Chlorophyta). Eur J Phycol 31: 349-359.
56. Porcar-Castell A, Pfündel E, Korhonen E, Juurola E (2008) A new monitoring PAM fluorometer (MONI-PAM) to study the short- and long-term acclimation of photosystem II in field conditions. Photosynth Res 96: 173-179.
57. Raggio J, Pintado A, Vivas M, Sancho LG and others (2014) Continuous chlorophyll fluorescence, gas exchange and microclimate monitoring in a natural soil crust habitat in Tabernas badlands, Almería, Spain: progressing towards a model to understand productivity. Biodivers Conserv 23: 1809-1826.
58. Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to asses photosynthetic activity. Aquat Bot 82: 222-237.
59. Ramírez T, Cortés D, Mercado JM, Vargas-Yáñez M, Sebastián M, Liger E (2005) Seasonal dynamics of in - organic nutrients and phytoplankton biomass in the NW Alboran Sea. Estuar Coast Shelf Sci 65: 654-670.
60. Raven JA (2011) Effects on marine algae of changed sea - water chemistry with increasing atmospheric CO2. Biol Environ Proc R Ir Acad B 111: 1-17.
61. Raven JA, Cockell CS, La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc Lond B Biol Sci 363: 2641-2650.
62. Renger G, Schreiber U (1986) Practical applications of fluo - rometric methods to algae and higher plant research. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, Orlando, FL, p 589-619.
63. Riebesell U, Schulz KG, Bellerby RGJ, Botros B and others (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450: 545-548.
64. Ritchie RJ (2008) Fitting light saturation curves measured using modulated fluorometry. Photosynth Res 96: 201-215.
65. Roleda MY, Hurd CL (2012) Seaweed responses to ocean acidification. In: Wiencke C, Bischof K (eds) Seaweed biology. Springer, Berlin, p 407-431.
66. Rüdiger W, López-Figueroa F (1992) Photoreceptors in algae. Annu Rev Photochem Photobiol 55: 949-954.
67. Runcie JW, Paulo D, Santos R, Sharon Y, Beer S, Silva J (2009) Photosynthetic responses of Halophila stipulacea to a light gradient. I. In situ energy partitioning of nonphotochemical quenching. Aquat Biol 7: 143-152.
68. Russell BD, Connell SD (2012) Origins and consequences of global and local stressors: incorporating climatic and non-climatic phenomena that buffer or accelerate ecological change. Mar Biol 159: 2633-2639.
69. Schreiber U, Bilger W (1993) Progress in chlorophyll fluo - rescence research: major developments during the past year in retrospect. In: Lüttge H, Ziegler HE (eds) Progress in botany, Vol 54. Springer, Berlin, p 151-173.
70. Stengel DB, Conde-Álvarez R, Connan S, Nitschke U and others (2014) Short-term effects of CO2, nutrients and temperature on three marine macroalgae under solar radiation. Aquat Biol 22: 159–176.
71. Underwood T (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge.
72. Vergara JJ, Bird KT, Niell FX (1995) Nitrogen assimilation following NH4+ pulses in the red alga Gracilariopsis lema nei formis: effect on C metabolism. Mar Ecol Prog Ser 122: 253-263.
73. Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oeco-logia 17: 281-291.
74. Zar JH (2009) Biostatistical analysis. Prentice Hall, Princeton, NJ.