Evaluating the effect of temperature on photosynthesis and respiration of articulated coralline algae using oxygen evolution and chlorophyll a fluorescence
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Abstract
Coralline algae form abundant and ecologically important submerged aquatic vegetation habitats throughout the world. However, algal performance is threatened by climate change and ocean acidification. Previous studies suggest that their photosynthetic performance will be compromised mainly at elevated temperatures. Understanding the impact of diverse climate change scenarios requires a clear and thorough comprehension of the photosynthetic response to temperature gradients. The objective of this study was to evaluate the short-term effect of temperature (10–35 °C) on the gross photosynthesis (GPS), respiration, and electron transport rates (ETRs) of 3 articulated coralline algae (Lithothrix aspergillum, Corallina officinalis, and Bossiella orbigniana) for a better understanding of their metabolism and to investigate the relationship between GPS and ETR as a function of temperature. The results showed that the coralline algal metabolism is highly sensitive to temperature, but responses were species-specific and can be related to their light adaptation/acclimation; the high-light-adapted L. aspergillum was least negatively affected. The photosynthesis to respiration ratio was optimal between 20 and 25 °C according to the local thermal regime but was significantly reduced toward higher temperatures, indicating strong carbon imbalances and highlighting the relevance of thermal stress for coralline algal performance. A strong correlation between GPS and ETR was found between 10 and 30 °C in all species, but both above saturation irradiances and at elevated temperatures (≥30 °C), a clear deviation from linearity occurred. This suggests that ETR is not a good proxy to estimate photosynthetic activity under light or thermal stress. This information should be useful for studies implementing global change scenarios and pulse amplitude modulated (PAM) fluorometry in coralline algae.
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References
Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci. 8(7):343–351.
https://doi.org/10.1016/S1360-1385(03)00136-5
Beer S, Axelsson L. 2004. Limitations in the use of PAM fluorometry for measuring photosynthetic rates of macroalgae at high irradiances. Eur J Phycol. 39(1):1–7.
https://doi.org/10.1080/0967026032000157138
Borlongan IA, Gerung GS, Kawaguchi S, Nishihara GN, Terada R. 2017. Thermal and PAR effects on the photosynthesis of Eucheuma denticulatum and Kappaphycus striatus (so-called Sacol strain) cultivated in shallow bottom of Bali, Indonesia. J Appl Phycol. 29:395–404.
https://doi.org/10.1007/s10811-016-0956-7
Borlongan IA, Suzuki S, Nishihara GN, Kozono J, Terada R. 2020. Effects of light quality and temperature on the photosynthesis and pigment content of a subtidal edible red alga Meristotheca papulosa (Solieriaceae, Gigartinales) from Japan. J Appl Phycol. 32(2):1329–1340.
https://doi.org/10.1007/s10811-020-02045-z
Cabello-Pasini A, Aguirre-von-Wobeser E, Figueroa FL. 2000. Photoinhibition of photosynthesis in Macrocystis pyrifera (Phaeophyceae), Chondrus crispus (Rhodophyceae) and Ulva lactuca (Chlorophyceae) in outdoor culture systems. J Photochem Photobiol B. 57(2–3):169–178.
https://doi.org/10.1016/S1011-1344(00)00095-6
Cabello-Pasini A, Figueroa FL. 2005. Effect of nitrate concentration on the relationship between photosynthetic oxygen evolution and electron transport rate in Ulva rigida (Chlorophyta). J Phycol. 41(6):1169–1177.
https://doi.org/10.1111/j.1529-8817.2005.00144.x
Cabello-Pasini A, Muñiz-Salazar R, Ward DH. 2004. Caracterización bioquímica del pasto marino Zostera marina en el límite sur de su distribución en el Pacífico Norte = Biochemical characterization of the eelgrass Zostera marina at its southern distribution limit in the North Pacific. Cienc Mar. 30(1A):21–34.
https://doi.org/10.7773/cm.v30i11.123
Cabello-Pasini A, Zertuche-González JA, Pacheco-Ruíz I. 2003. Photosynthesis, growth and nitrogen uptake of competing marine macrophytes in the Gulf of California. Bot Mar. 46(6).
https://doi.org/10.1515/BOT.2003.052
Carr H, Bjork M. 2003. A methodological comparison of photosynthetic oxygen evolution and estimated electron transport rate in tropical Ulva (Chlorophyceae) species under different light and inorganic carbon conditions. J Phycol. 39(6):1125–1131.
https://doi.org/10.1111/j.0022-3646.2003.02-077.x
Chisholm JRM. 2000. Calcification by crustose coralline algae on the northern Great Barrier Reef, Australia. Limnol Oceanogr. 45(7):1476–1484.
https://doi.org/10.4319/lo.2000.45.7.1476
Colombo‐Pallotta MF, García‐Mendoza E, Ladah LB. 2006. Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol. 42(6):1225–1234.
https://doi.org/10.1111/j.1529-8817.2006.00287.x
Díaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O. 2012. Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. J Phycol. 48(1):32–39.
https://doi.org/10.1111/j.1529-8817.2011.01084.x
Edwards GE, Baker NR. 1993. Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynth Res. 37:89–102.
https://doi.org/10.1007/bf02187468
Eggert A. 2012. Seaweed Responses to Temperature. In: Wiencke C, Bischof K (eds.), Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization. Berlin, Heidelberg (Germany): Springer. 47–66.
https://doi.org/10.1007/978-3-642-28451-9_3
Falkowski PG, Raven JA. 2007. Aquatic Photosynthesis. United States of America: Princeton University Press. 512 p.
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.
https://doi.org/10.1023/A:1023936313544
Foster MS. 2001. Rhodoliths: between rocks and soft places. J Phycol. 37(5):659–667.
https://doi.org/10.1046/j.1529-8817.2001.00195.x
Foster MS, Riosmena-Rodríguez R, Steller DL, Woelkerling WJ. 1997. Living rhodoliths beds in the Gulf of California and their implications for paleoenvironmental interpretation. Spec Pap Geol Soc Am. 318:127–139.
https://doi.org/10.1130/0-8137-2318-3.127
Franklin LA, Badger MR. 2001. A comparison of photosynthetic electron transport rates in macroalgae measured by pulse amplitude modulated chlorophyll fluorometry and mass spectrometry. J Phycol. 37(5):756–767.
https://doi.org/10.1046/j.1529-8817.2001.00156.x
Gefen-Treves S, Kedem I, Weiss G, Wagner D, Tchernov D, Kaplan A. 2020. Acclimation of a rocky shore algal reef builder Neogoniolithon sp. to changing illuminations. Limnol Oceanogr. 65(1):27–36.
https://doi.org/10.1002/lno.11245
Guy-Haim T, Silverman J, Raddatz S, Wahl M, Israel A, Rilov G. 2016. The carbon turnover response to thermal stress of a dominant coralline alga on the fast warming Levant coast. Limnol Oceanogr. 61(3):1120–1133.
https://doi.org/10.1002/lno.10279
Hofmann LC, Yildiz G, Hanelt D, Bischof K. 2012. Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol. 159(4):783–792.
https://doi.org/10.1007/s00227-011-1854-9
Jernakoff P, Phillips BF, Fitzpatrick JJ. 1993. The diet of postpuerulus western rock lobster, Panulirus cygnus George, at Seven Mile Beach, Western Australia. Aust J Mar Fresh Res. 44(4):649–655.
https://doi.org/10.1071/MF9930649
Legrand E, Riera P, Bohner O, Coudret J, Schlicklin F, Derrien M, Martin S. 2018. Impact of ocean acidification and warming on the productivity of a rock pool community. Mar Environ Res. 136:78–88.
https://doi.org/10.1016/j.marenvres.2018.02.010
Linnane A, Ball B, Munday B, Mercer JP. 2000. On the occurrence of juvenile lobster Homarus gammarus in intertidal habitat. J Mar Biol Assoc UK. 80(2):375–376.
https://doi.org/10.1017/S0025315499002039
Longstaff BJ, Kildea T, Runcie JW, Cheshire A, Dennison WC, Hurd C, Kana T, Raven JA, Lurkum AWD. 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynth Res. 74(3):281–293.
https://doi.org/10.1023/a:1021279627409
Martin S, Castets M-D, Clavier J. 2006. Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquat Bot. 85(2):121–128.
https://doi.org/10.1016/j.aquabot.2006.02.005
Martin S, Gattuso J-P. 2009. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol. 15(8):2089–2100.
https://doi.org/10.1111/j.1365-2486.2009.01874.x
Martone PT, Alyono M, Stites S. 2010. Bleaching of an intertidal coralline alga: untangling the effects of light, temperature, and desiccation. Mar Ecol Prog Ser. 416:57–67.
https://doi.org/10.3354/meps08782
Maxwell K, Johnson GN. 2000. Chlorophyll fluorescence—a practical guide. J Exp Bot. 51(345):659–668.
https://doi.org/10.1093/jexbot/51.345.659
Newell RC, Pye VI. 1968. Seasonal variations in the effect of temperature on the respiration of certain intertidal algae. J Mar Biol Assoc UK. 48(2):341–348.
https://doi.org/10.1017/s0025315400034536
Orzymski J, Johnsen G, Sakshaug E. 1997. The significance of intracellular self-shading on the biooptical properties of brown, red, and green macroalgae. J Phycol. 33(3):408–414.
https://doi.org/10.1111/j.0022-3646.1997.00408.x
Peña-Manjarrez JL, Gaxiola-Castro G, Helenes-Escamilla J. 2009. Environmental factors influencing the variability of Lingulodinium polyedrum and Scrippsiella trochoidea (Dinophyceae) cyst production = Factores ambientales que influyen en la variabilidad de la producción de quistes de Lingulodinium polyedrum y Scrippsiella trochoidea (Dinophyceae). Cienc Mar. 35(1):1–14.
https://doi.org/10.7773/cm.v35i1.1406
Rendina F, Bouchet PJ, Appolloni L, Russo GF, Sandulli R, Kolzenburg R, Putra A, Ragazzola F. 2019. Physiological response of the coralline alga Corallina officinalis L. to both predicted long-term increases in temperature and short-term heatwave events. Mar Environ Res. 150:104764.
https://doi.org/10.1016/j.marenvres.2019.104764
Schreiber U. 2004. Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee (eds.), Chlorophyll a Fluorescence. Advances in Photosynthesis and Respiration Vol. 19. Dordrecht (Netherlands): Springer Netherlands. 279–319.
https://doi.org/10.1007/978-1-4020-3218-9_11
Schubert N, García-Mendoza E. 2008. Photoinhibition in red algal species with different carotenoid profiles. J Phycol. 44(6):1437–1446.
https://doi.org/10.1111/j.1529-8817.2008.00590.x
Schubert N, García-Mendoza E, Enríquez S. 2011. Is the photoacclimatory response of Rhodophyta conditioned by the species carotenoid profile? Limnol Oceanogr. 56(6):2347– 2361.
https//doi.org/10.4319/lo.2011.56.6.2347
Sordo L, Santos R, Barrote I, Freitas C, Silva J. 2020. Seasonal photosynthesis, respiration, and calcification of a temperate maërl bed in southern Portugal. Front Mar Sci. 7:136.
https://doi.org/10.3389/fmars.2020.00136
Steller DL, Riosmena-Rodríguez R, Foster MS, Roberts CA. 2003. Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquatic Conserv: Mar Freshw Ecosyst. 13(S1):S5–S20.
https://doi.org/10.1002/aqc.564
Vásquez-Elizondo RM, Legaria-Moreno L, Perez-Castro MÁ, Krämer WE, Scheufen T, Iglesias-Prieto R, Enriquez S. 2017. Absorptance determinations on multicellular tissues. Photosynth Res. 132:311–324.
https://doi.org/10.1007/s11120-017-0395-6
Vásquez-Elizondo RM, Enríquez S. 2016. Coralline algal physiology is more adversely affected by elevated temperature than reduced pH. Sci Rep. 6:19030.
https://doi.org/10.1038/srep19030
Vásquez-Elizondo RM, Enríquez S. 2017. Light absorption in coralline algae (Rhodophyta): A morphological and functional approach to understanding species distribution in a coral reef lagoon. Front Mar Sci. 4:297.
https://doi.org/10.3389/fmars.2017.00297
Webster NS, Soo R, Cobb R, Negri AP. 2011. Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME J. 5:759–770.
https://doi.org/10.1038/ismej.2010.152
Williamson CJ, Perkins R, Voller M, Yallop ML, Brodie J. 2017. The regulation of coralline algal physiology, an IN SITU study of Corallina officinalis (Corallinales, Rhodophyta). Biogeosciences. 14(19):4485–4498.