Skip to main content

Interactions between P-limitation and different C conditions on the fatty acid composition of an extremophile microalga

Abstract

The extremophilic microalga Chlamydomonas acidophila inhabits very acidic waters (pH 2–3.5), where its growth is often limited by phosphorus (P) or colimited by P and inorganic carbon (CO2). Because this alga is a major food source for predators in acidic habitats, we studied its fatty acid content, which reflects their quality as food, grown under a combination of P-limited and different carbon conditions (either mixotrophically with light + glucose or at high or low CO2, both without glucose). The fatty acid composition largely depended on the cellular P content: stringent P-limited cells had a higher total fatty acid concentration and had a lower percentage of polyunsaturated fatty acids. An additional limitation for CO2 inhibited this decrease, especially reflected in enhanced concentrations of 18:3(9,12,15) and 16:4(3,7,10,13), resulting in cells relatively rich in polyunsaturated fatty acids under colimiting growth conditions. The percentage of polyunsaturated to total fatty acid content was positively related with maximum photosynthesis under all conditions applied. The two factors, P and CO2, thus interact in their effect on the fatty acid composition in C. acidophila, and colimited cells P-limited algae can be considered a superior food source for herbivores because of the high total fatty acid content and relative richness in polyunsaturated fatty acids.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

Alpha (α):

Initial slope of the photosynthesis–irradiance curve

ANCOVA:

Analysis of covariance

Beta (β):

Slope at high irradiances that describes photo-inhibition

DGDG:

Digalactosyldiacylglycerol

FA:

Fatty acid

I:

Actinic light intensity

K m(CO2) :

Half saturation constant for CO2 uptake

μ:

Growth rate

MUFA:

Monounsaturated fatty acid

Mixotrophy:

Growth on glucose and light

P:

Phosphorus

Pr:

Photosynthetic rate

P max :

Maximum photosynthetic rate

PUFA:

Polyunsaturated fatty acid

Q p :

Cellular P quota

R d :

Dark respiration rate

SFA:

Saturated fatty acid

References

  1. Ahlgren G, Goedkoop W, Markensten H, Sonesten L, Boberg M (1997) Seasonal variations in food quality for pelagic and benthic invertebrates in Lake Erken—the role of fatty acids. Freshw Biol 38:555–570

    Article  CAS  Google Scholar 

  2. Ahlgren G, Zeipel K, Gustafsson I-B (1998) Phosphorus limitation effects on the fatty acid content and nutritional quality of a green alga and a diatom. Verh int Ver Limnol 26:1659–1664

    CAS  Google Scholar 

  3. Amoroso G, Sültemeyer D, Thyssen C, Fock HP (1998) Uptake of HCO3 and CO2 in cells and chloroplasts from the microalgae Chlamydomonas reinhardtii and Dunaliella tertiolecta. Plant Physiol 116:193–201

    Article  CAS  Google Scholar 

  4. Andersson MX, Stridh MH, Larsson KE, Lijenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132

    PubMed  Article  CAS  Google Scholar 

  5. Arisz SA, van Himbergen JAJ, Musgrave A, van den Ende H, Munnik T (2000) Polar glycerolipids of Chlamydomonas moewusii. Phytochemistry 53:265–270

    PubMed  Article  CAS  Google Scholar 

  6. Arts MT, Kohler CC (2009) Health and condition in fish: the influence of lipids on membrane competency and immune response. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 237–255

    Chapter  Google Scholar 

  7. Awai K, Watanabe H, Benning C, Nishida I (2007) Digalactosyldiacylglycerol is required for better photosynthetic growth of Synechocystis sp PCC6803 under phosphate limitation. Plant Cell Physiol 48:1517–1523

    PubMed  Article  CAS  Google Scholar 

  8. Boëchat IG, Weithoff G, Krüger A, Gücker B, Adrian R (2007) A biochemical explanation for the success of mixotrophy in the flagellate Ochromonas sp. Limnol Oceanogr 52:1624–1632

    Article  Google Scholar 

  9. Dijkman NA, Kromkamp JC (2006) Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition. Mar Ecol Prog Ser 324:113–125

    Article  CAS  Google Scholar 

  10. Eichenberger W (1976) Lipids of Chlamydomonas reinhardi under different growth conditions. Phytochemistry 15:459–463

    Article  CAS  Google Scholar 

  11. Ekman A, Bulow L, Stymne S (2007) Elevated atmospheric CO2 concentration and diurnal cycle induce changes in lipid composition in Arabidopsis thaliana. New Phytol 174:591–599

    PubMed  Article  CAS  Google Scholar 

  12. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    PubMed  Article  Google Scholar 

  13. Giroud C, Gerber A, Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol 29:587–595

    CAS  Google Scholar 

  14. Guiheneuf F, Mimouni V, Ulmann L, Tremblin G (2009) Combined effects of irradiance level and carbon source on fatty acid and lipid class composition in the microalga Pavlova lutheri commonly used in mariculture. J Exp Mar Biol Ecol 369:136–143

    Article  CAS  Google Scholar 

  15. Guschina IA, Harwood JL (2009) Algal lipids and effect of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 1–24

    Chapter  Google Scholar 

  16. Hartwich M, Wacker A, Weithoff G (2010) Changes in the competitive abilities of two rotifers feeding on mixotrophic flagellates. J Plankton Res 32:1727–1731

    Article  Google Scholar 

  17. Hu HH, Gao KS (2003) Optimization of growth and fatty acid composition of a unicellular marine picoplankton. Nannochloropsis sp., with enriched carbon sources. Biotechnol Lett 25:421–425

    PubMed  Article  CAS  Google Scholar 

  18. Kamjunke N, Gaedke U, Tittel J, Weithoff G, Bell EM (2004) Strong vertical differences in the plankton composition of an extremely acidic lake. Arch Hydrobiol 161:289–306

    Article  Google Scholar 

  19. Kehr J, Wagner C, Willmitzer L, Fisahn J (1999) Effect of modified carbon allocation on turgor, osmolality, sugar and potassium content, and membrane potential in the epidermis of transgenic potato (Solanum tuberosum L.) plants. J Exp Bot 50:565–571

    Article  CAS  Google Scholar 

  20. Khozin-Goldberg I, Cohen Z (2006) The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67:696–701

    PubMed  Article  CAS  Google Scholar 

  21. Lukas M, Sperfeld E, Wacker A (2011) Growth rate hypothesis does not apply across co-limiting conditions: cholesterol limitation affects phosphorus homeostasis of an aquatic herbivore. Funct Ecol. doi:10.1111/j.1365-2435.2011.01876.x

  22. Malzahn AM, Aberle N, Clemmesen C (2007) Nutrient limitation of primary producers affects planktivorous fish condition. Limnol Oceanogr 52:2062–2071

    Article  CAS  Google Scholar 

  23. Martin-Creuzburg D, Sperfeld E, Wacker A (2009) Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proc R Soc B Biol Sci 276:1805–1814

    Article  CAS  Google Scholar 

  24. Müller-Navarra DC (1995) Biochemical versus mineral limitation in Daphnia. Limnol Oceanogr 40:1209–1214

    Article  Google Scholar 

  25. Müller-Navarra DC, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77

    PubMed  Article  Google Scholar 

  26. Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Anal Chim Acta 26:31–36

    Article  Google Scholar 

  27. Nichols HW (1973) Growth media-freshwater. In: Stein JR (ed) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge, pp 7–24

    Google Scholar 

  28. Park S, Brett MT, Müller-Navarra DC, Goldman CR (2002) Essential fatty acid content and the phosphorus to carbon ratio in cultured algae as indicators of food quality for Daphnia. Freshw Biol 47:1377–1390

    Article  CAS  Google Scholar 

  29. Piepho M, Arts MT, Wacker A (2011) Species-specific variation in fatty acid concentrations of four phytoplankton species: does phosphorus supply influence the effect of light intensity and temperature? J Phycol (accepted)

  30. Poerschmann J, Spijkerman E, Langer U (2004) Fatty acid patterns in Chlamydomonas sp. as a marker for nutritional regimes and temperature under extremely acidic conditions. Microb Ecol 48:78–89

    PubMed  Article  CAS  Google Scholar 

  31. Pronina NA, Rogova NB, Furnadzhieva S, Klyachko-Gurvich GL (1998) Effect of CO2 concentration on the fatty acid composition of lipids in Chlamydomonas reinhardtii cia-3, a mutant deficient in CO2-concentrating mechanism. Russ J Plant Physiol 45:447–455

    CAS  Google Scholar 

  32. Riebesell U, Revill AT, Holdsworth DG, Volkman JK (2000) The effects of varying CO2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi. Geochim Cosmochim Acta 64:4179–4192

    Article  CAS  Google Scholar 

  33. Sakurai I, Mizusawa N, Wada H, Sato N (2007) Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol 145:1361–1370

    PubMed  Article  CAS  Google Scholar 

  34. Sato N (1989) Modulation of lipid and fatty acid content by carbon dioxide in Chlamydomonas reinhardtii. Plant Sci 61:17–21

    Article  CAS  Google Scholar 

  35. Sato N, Sonoike K, Tsuzuki M, Kawaguchi A (1996) Photosynthetic characteristics of a mutant of Chlamydomonas reinhardtii impaired in fatty acid desaturation in chloroplasts. Biochim Biophys Acta Bioenerg 1274:112–118

    Article  Google Scholar 

  36. Sato N, Tsuzuki M, Kawaguchi A (2003) Glycerolipid synthesis in Chlorella kessleri 11 h—II. Effect of the CO2 concentration during growth. Biochim Biophys Acta Mol Cell Biol Lipids 1633:35–42

    CAS  Google Scholar 

  37. Sperfeld E, Wacker A (2009) Effects of temperature and dietary sterol availability on growth and cholesterol allocation of the aquatic keystone species Daphnia. J Exp Biol 212:3051–3059

    PubMed  Article  CAS  Google Scholar 

  38. Spijkerman E (2007) Phosphorus acquisition by Chlamydomonas acidophila under autotrophic and osmo-mixotrophic growth conditions. J Exp Bot 58:4195–4202

    PubMed  Article  CAS  Google Scholar 

  39. Spijkerman E (2008a) Phosphorus limitation of algae living in iron-rich, acidic lakes. Aquat Microb Ecol 53:201–210

    Article  Google Scholar 

  40. Spijkerman E (2008b) What physiological acclimation supports increased growth at high CO2 conditions? Physiol Plantarum 133:41–48

    Article  CAS  Google Scholar 

  41. Spijkerman E (2010) High photosynthetic rates under a co-limitation for inorganic phosphorus and carbon dioxide. J Phycol 46:658–664

    Article  CAS  Google Scholar 

  42. Sterner R (2008) On the phosphorus limitation paradigm for lakes. Int Rev Hydrobiol 93:433–445

    Article  CAS  Google Scholar 

  43. Thompson GA (1996) Lipids and membrane function in green algae. Biochim Biophys Acta Lipids Lipid Metab 1302:17–45

    Article  Google Scholar 

  44. Tittel J, Bissinger V, Zippel B, Gaedke U, Bell E, Lorke A, Kamjunke N (2003) Mixotrophs combine resource use to outcompete specialists: Implications for aquatic food webs. Proc Natl Acad Sci USA 100:12776–12781

    PubMed  Article  CAS  Google Scholar 

  45. Tittel J, Bissinger V, Gaedke U, Kamjunke N (2005) Inorganic carbon limitation and mixotrophic growth in Chlamydomonas from an acidic mining lake. Protist 156:63–75

    PubMed  Article  CAS  Google Scholar 

  46. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184

    Article  CAS  Google Scholar 

  47. Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45:744–750

    Article  CAS  Google Scholar 

  48. Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblizek M, Lomas MW, Mincer TJ, Moore LR, Moutin T, Rappe MS, Webb EA (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72

    PubMed  Article  Google Scholar 

  49. Villar-Argaiz M, Medina-Sanchez JM, Bullejos FJ, Delgado-Molina JA, Perez OR, Navarro JC, Carrillo P (2009) UV radiation and phosphorus interact to influence the biochemical composition of phytoplankton. Freshw Biol 54:1233–1245

    Article  CAS  Google Scholar 

  50. Villarejo A, Orus MI, Martinez F (1995) Coordination of photosynthetic and respiratory metabolism in Chlorella vulgaris UAM-101 in the light. Physiol Plantarum 94:680–686

    Article  CAS  Google Scholar 

  51. Wacker A, Martin-Creuzburg D (2007) Allocation of essential lipids in Daphnia magna during exposure to poor food quality. Funct Ecol 21:738–747

    Article  Google Scholar 

  52. Wacker A, Von Elert E (2001) Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82:2507–2520

    Google Scholar 

  53. Wacker A, Weithoff G (2009) Carbon assimilation mode in mixotrophs and the fatty acid composition of their rotifer consumers. Freshw Biol 54:2189–2199

    Article  CAS  Google Scholar 

  54. Weers PMM, Gulati RD (1997) Growth and reproduction of Daphnia galeata in response to changes in fatty acids, phosphorus, and nitrogen in Chlamydomonas reinhardtii. Limnol Oceanogr 42:1584–1589

    Article  CAS  Google Scholar 

  55. Weithoff G, Wacker A (2007) The mode of nutrition of mixotrophic flagellates determines the food quality for their consumers. Funct Ecol 21:1092–1098

    Article  Google Scholar 

  56. Wolowski K, Turnau K, Henriques FS (2008) The algal flora of an extremely acidic, metal-rich drainage pond of Sao Domingos pyrite mine (Portugal). Cryptogamie Algol 29:313–324

    Google Scholar 

  57. Yamamoto Y, Tatsuzawa H, Wada M (1998) Effect of environmental conditions on the composition of lipids and fatty acids in Chlamydomonas isolated from an acidic lake. Verh Int Ver Theor Angew Limnol 26:1788–1790

    CAS  Google Scholar 

  58. Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall/Pearson Education, London

    Google Scholar 

Download references

Acknowledgments

This work has been supported by the German research foundation (DFG, SP695/2 and SP695/4) to ES and (WA2445/4-1) to AW. We greatly acknowledge the technical assistance of Silvia Heim and Cathleen Friedrich.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Elly Spijkerman.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 38 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Spijkerman, E., Wacker, A. Interactions between P-limitation and different C conditions on the fatty acid composition of an extremophile microalga. Extremophiles 15, 597 (2011). https://doi.org/10.1007/s00792-011-0390-3

Download citation

Keywords

  • Acidophilic algae
  • Cellular P quota
  • Chlamydomonas acidophila
  • Chlorophyceae
  • Colimitation
  • CO2
  • Fatty acid composition
  • Food quality
  • Glucose
  • Mixotrophy
  • Photosynthesis
  • Phytoplankton
  • Phosphorus limitation