Effects of temperature and salinity on respiratory losses and the ratio of photosynthesis to respiration in representative Antarctic phytoplankton species

Autoři: Deborah Bozzato aff001;  Torsten Jakob aff001;  Christian Wilhelm aff002
Působiště autorů: University Leipzig, Institute of Biology, Plant Physiology, Leipzig, Germany aff001;  Saxon Institute of Biotechnology, Leipzig, Germany aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224101


The Southern Ocean (SO) is a net sink for atmospheric CO2 whereby the photosynthetic activity of phytoplankton and sequestration of organic carbon (biological pump) plays an important role. Global climate change will tremendously influence the dynamics of environmental conditions for the phytoplankton community, and the phytoplankton will have to acclimate to a combination of changes of e.g. water temperature, salinity, pH, and nutrient supply. The efficiency of the biological pump is not only determined by the photosynthetic activity but also by the extent of respiratory carbon losses of phytoplankton cells. Thus, the present study investigated the effect of different temperature and salinity combinations on the ratio of gross photosynthesis to respiration (rGP/R) in two representative phytoplankton species of the SO. In the comparison of phytoplankton grown at 1 and 4°C the rGP/R decreased from 11.5 to 7.7 in Chaetoceros sp., from 9.1 to 3.2 in Phaeocystis antarctica strain 109, and from 12.4 to 7.0 in P. antarctica strain 764, respectively. The decrease of rGP/R was primarily dependent on temperature whereas salinity was only of minor importance. Moreover, the different rGP/R at 1 and 4°C were caused by changes of temperature-dependent respiration rates but were independent of changes of photosynthetic rates. For further interpretation, net primary production (NPP) was calculated for different seasonal conditions in the SO with specific combinations of irradiance, temperature, and salinity. Whereas, maximum photosynthetic rates significantly correlated with calculated NPP under experimental ‘Spring’, ‘Summer’, and ‘Autumn’ conditions, there was no correlation between rGP/R and the respective values of NPP. The study revealed species-specific differences in the acclimation to temperature and salinity changes that could be linked to their different original habitats.

Klíčová slova:

Light – Oxygen – Photosynthesis – Phytoplankton – Salinity – Sea ice – Seasons – Spring


1. Raven JA, Falkowski PG. Oceanic sinks for atmospheric CO2. Plant, Cell and Environment. 1999;22: 741–755.

2. Siegel DA, Buesseler KO, Doney SC, Sailley SF, Behrenfeld MJ, Boyd PW. Global assessment of ocean carbon export by combining satellite observations and food-web models. Global Biogeochem Cycles. 2014;28: 2013GB004743

3. Turner J, Barrand NE, Bracegirdle TJ, Convey P, Hodgson DA, Jarvis M, et al. Antarctic climate change and the environment: an update. Polar Record. 2014;50: 237–259.

4. Deppeler SL, Davidson AT. Southern Ocean phytoplankton in a changing climate. Front Mar Sci. 2017;4. doi: 10.3389/fmars.2017.00040

5. Tortell PD, Payne CD, Li Y, Trimborn S, Rost B, Smith WO, Riesselman C, Dunbar RB, Sedwick P, DiTullio GR. CO2 sensitivity of Southern Ocean phytoplankton. Geophys Res Lett. 2008. doi: 10.1029/2008gl035090

6. Petrou K, Kranz SA, Trimborn S, Hassler CS, Ameijeiras SB, Sackett O, Ralph PJ, Davidson AT. Southern Ocean phytoplankton physiology in a changing climate. J Plant Physiol. 2016;203: 135–150. doi: 10.1016/j.jplph.2016.05.004 27236210

7. Kennicutt MC, Chown SL, Cassano JJ, Liggett D, Peck LS, Massom R, et al. A roadmap for Antarctic and Southern Ocean science for the next two decades and beyond. Antarctic Science. 2015;27: 3–18.

8. Xavier JC, Brandt A, Ropert-Coudert Y, Badhe R, Gutt J, Havermans C, Jones C, et al. Future Challenges in Southern Ocean Ecology Research. Front Mar Sci. 2016. doi: 10.3389/fmars.2016.00094

9. Arístegui J, Montero MF, Ballesteros S, Basterretxea G, van Lenning K. Planktonic primary production and microbial respiration measured by 14C assimilation and dissolved oxygen changes in coastal waters of the Antarctic Peninsula during austral summer: implications for carbon flux studies. Mar Ecol Prog Ser. 1996;132: 191–201.

10. Petrou K, Ralph PJ. Photosynthesis and net primary productivity in three Antarctic diatoms: possible significance for their distribution in the Antarctic marine ecosystem. Mar Ecol Prog Ser. 2011;437: 27–40.

11. Tilzer MM, Dubinsky Z. Effects of temperature and day length on the mass balance of Antarctic phytoplankton. Polar Biol. 1987;7: 35–42.

12. Marra J. Net and gross productivity: weighing in with 14C. Aquat Microb Ecol. 2009;56: 123–131

13. Regaudie‐de‐Gioux A, Duarte CM. Temperature dependence of planktonic metabolism in the ocean. Global Biogeochem Cycles. 2012. doi: 10.1029/2010GB003907

14. Lancelot C, Billen G, Veth C, Becquevort S, Mathot S. Modelling carbon cycling through phytoplankton and microbes in the Scotia—Weddell Sea area during sea ice retreat. Mar Chem. 1991;35: 305–324.

15. Gogorev RM, Samsonov NI. The genus Chaetoceros (Bacillariophyta) in Arctic and Antarctic. Novosti Sist Nizsh Rast. 2016;50: 56–111.

16. Rembauville M, Manno C, Tarling GA, Blain S, Salter I. Strong contribution of diatom resting spores to deep-sea carbon transfer in naturally iron-fertilized waters downstream of South Georgia. Deep Sea Research Part I: Oceanographic Research Papers. 2016;115: 22–35.

17. Arrigo KR, Mills MM, Kropuenske LR, Dijken GL van, Alderkamp A-C, Robinson DH. Photophysiology in two major Southern Ocean phytoplankton taxa: Photosynthesis and growth of Phaeocystis antarctica and Fragilariopsis cylindrus under different irradiance levels. Integr Comp Biol. 2010;50: 950–966. doi: 10.1093/icb/icq021 21558252

18. Kropuenske LR, Mills MM, van Dijken GL, Bailey S, Robinson DH, Welschmeyer NA, et al. Photophysiology in two major Southern Ocean phytoplankton taxa: photoprotection in Phaeocystis antarctica and Fragilariopsis cylindrus. Limnol Oceanogr. 2009;54: 1176.

19. Gäbler-Schwarz S, Medlin LK, Leese F. A puzzle with many pieces: the genetic structure and diversity of Phaeocystis antarctica Karsten (Prymnesiophyta). Eur J Phycol. 2015;50: 112–124.

20. Loeblich AR, Smith VE. Chloroplast pigments of the marine dinoflagellate Gyrodinium resplendens. Lipids. 1968;3: 5. doi: 10.1007/BF02530961 17805834

21. Jeffrey SW, Humphrey GF. New spectrometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz. 1975;167: 191–194.

22. Wagner H, Jakob T, Wilhelm C. Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol. 2006;169: 95–108. doi: 10.1111/j.1469-8137.2005.01550.x 16390422

23. Benson BB, Krause D. The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere1. Limnol Oceanogr. 1984; 29: 620–632.

24. Beardall J, Burger-Wiersma T, Rijkeboe M, Sukenik A, Lemoalle J, Dubinsky Z, et al. Studies on enhanced post-illumination respiration in microalgae. J Plankton Res. 1994;16: 1401–1410.

25. Genty B, Briantais J-M, Baker NR. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta. 1989;990: 87–92.

26. Schreiber U, Neubauer C. O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res. 1990;25: 279–293. doi: 10.1007/BF00033169 24420358

27. Streb P, Josse EM, Gallouet E, Baptist F, Kuntz M, Cornic G. Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Envir. 2005;28: 1123–1135.

28. Bailey S, Melis A, Mackey KR, Cardol P, Finazzi G, van Dijken G, et al. Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta. 2008;1777: 269–76. doi: 10.1016/j.bbabio.2008.01.002 18241667

29. Eilers PHC, Peeters JCH. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model. 1988;42: 199–215.

30. Schreiber U, Bilger W, Neubauer C. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM, editors. Ecophysiology of photosynthesis. Berlin Heidelberg: Springer; 1994. pp. 49–70.

31. Serôdio J, Lavaud J. A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res. 2011;108: 61–76. doi: 10.1007/s11120-011-9654-0 21516348

32. Gilbert M, Wilhelm C, Richter M. Bio-optical modelling of oxygen evolution using in vivo fluorescence: comparison of measured and calculated photosynthesis/irradiance (P-I) curves in four representative phytoplankton species. J Plant Physiol. 2000;157: 307–314.

33. Thomas DN, Baumann MEM, Gleitz M. Efficiency of carbon assimilation and photoacclimation in a small unicellular Chaetoceros species from the Weddell Sea (Antarctica): Influence of temperature and irradiance. J Exp Mar Biol Ecol. 1992;157: 195–209.

34. Kranz SA, Young JN, Hopkinson BM, Goldman JAL, Tortell PD, Morel FMM. Low temperature reduces the energetic requirement for the CO2 concentrating mechanism in diatoms. New Phytol. 2015;205: 192–201. doi: 10.1111/nph.12976 25308897

35. Young JN, Goldman JAL, Kranz SA, Tortell PD, Morel FMM. Slow carboxylation of Rubisco constrains the rate of carbon fixation during Antarctic phytoplankton blooms. New Phytol. 2015;205: 172–181. doi: 10.1111/nph.13021 25283055

36. Lizotte MP. The contributions of sea ice algae to Antarctic marine primary production. Integr Comp Biol. 2001;41: 57–73.

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

38. Petrou K, Trimborn S, Rost B, Ralph PJ, Hassler CS. The impact of iron limitation on the physiology of the Antarctic diatom Chaetoceros simplex. Mar Biol. 2014;161: 925–937. doi: 10.1007/s00227-014-2392-z 24719494

39. Alderkamp AC, Kulk G, Buma AGJ, Visser RJW, Van Dijken GL, Mills MM, et al. The effect of iron limitation on the photophysiology of Phaeocystis antarctica (prymnesiophyceae) and Fragilariopsis cylindrus (bacillariophyceae) under dynamic irradiance. J Phycol. 2012;48: 45–59. doi: 10.1111/j.1529-8817.2011.01098.x 27009649

40. Taddei L, Chukhutsina VU, Lepetit B, Stella GR, Bassi R, van Amerongen H, et al. Dynamic changes between two LHCX-related energy quenching sites control diatom photoacclimation, Plant Physiol. 2018, doi: 10.1104/pp.18.00448 29773581

41. Schellenberger Costa B, Jungandreas A, Jakob T, Weisheit W, Mittag M, Wilhelm C. Blue light is essential for high light acclimation and photoprotection in the diatom Phaeodactylum tricornutum. J Exp Bot. 2013;64: 483–493. doi: 10.1093/jxb/ers340 23183259

42. Halsey KH, Jones BM. Phytoplankton strategies for photosynthetic energy allocation. Ann Rev Mar Sci. 2015;7: 265–297. doi: 10.1146/annurev-marine-010814-015813 25149563

43. Wagner H, Jakob T, Fanesi A, Wilhelm C. Towards an understanding of the molecular regulation of carbon allocation in diatoms: the interaction of energy and carbon allocation. Phil Trans R Soc B. 2017;372: 20160410. doi: 10.1098/rstb.2016.0410 28717020

44. Kirk JTO. Light and photosynthesis in aquatic ecosystems, 1st ed. New York: Cambridge University Press; 1994.

Článek vyšel v časopise


2019 Číslo 10