Copper excess-induced large reversible and small irreversible adaptations in a population of Chlamydomonas reinhardtii CW15 (Chlorophyta)

• Autorzy: Plucinski B. , Waloszek A. , Rutkowska J. , Strzalka K.
• Języki publikacji: EN

Abstrakty

EN

Two Chlamydomonas reinhardtii CW15 populations modified by an excess of copper in growth medium were obtained: a “Cu” population that was continuously grown under the selection pressure of 5 μM Cu²⁺ (for at least 48 weeks) and the “Re” population, where a relatively short (9 week) exposure to elevated copper, necessary for acquiring tolerance, was followed by a prolonged period (at least 39 weeks) of cultivation at a normal (0.25 μM) copper concentration. Cells of the Cu population were able to multiply at a Cu²⁺ concentration 16 times higher than that of the control population at a normal light intensity and at a Cu²⁺ concentration 64 times higher when cultivated in dim light. The potential quantum yield of photosystem II (FV/FM ratio) under copper stress was also significantly higher for the Cu population than for Re and control populations. The Re population showed only residual tolerance towards the elevated concentration of copper, which is revealed by an FV/FM ratio slightly higher than in the control population under Cu²⁺ stress in dim light or in darkness. We postulate that in the Chlamydomonas populations studied in this paper, at least two mechanisms of copper tolerance operate. The first mechanism is maintained during cultivation at a standard copper concentration and seems to be connected with photosynthetic apparatus. This mechanism, however, has only low adaptive value under excess of copper. The other mechanism, with a much higher adaptive value, is probably connected with Cu²⁺ homeostasis at the cellular level, but is lost during cultivation at a normal copper concentration.

• Wydawca: -
• Czasopismo: Acta Societatis Botanicorum Poloniae
• Rocznik: 2018
• Tom: 87
• Numer: 1
• Opis fizyczny: Article 3569 [18p.],fig.,ref.

Twórcy

autor

Plucinski B.

• Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland

autor

Waloszek A.

• Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland

autor

Rutkowska J.

• Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland

autor

Strzalka K.

• Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland
• Malopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387 Krakow, Poland

Bibliografia

• 1. Nagajyoti PC, Lee KD, Sreekanth TVM. Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett. 2010;8:199–216. https://doi.org/10.1007/s10311-010-0297-8
• 2. Marschner H. Mineral nutrition of higher plants. London: Academic Press; 1995.
• 3. Holm RH, Kennepohl P, Solomon EI. Structural and functional aspects of metal sites in biology. Chem Rev. 1996;96(7):2239–2314. https://doi.org/10.1021/cr9500390
• 4. Festa RA, Thiele DJ. Copper: an essential metal in biology. Curr Biol. 2011;21:877–883. https://doi.org/10.1016/j.cub.2011.09.040
• 5. Quinn JM, Eriksson M, Moseley JL, Merchant S. Oxygen deficiency responsive gene expression in Chlamydomonas reinhardtii through a copper-sensing signal transduction pathway. Plant Physiol. 2002;128:463–471. https://doi.org/10.1104/pp.010694
• 6. Palmer CM, Guerinot ML. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol. 2009;5:333–340. https://doi.org/10.1038/nchembio.166
• 7. Burkhead JL, Reynolds KAG, Abdel-Ghany SE, Cohu CM, Pilon M. Copper homeostasis. New Phytol. 2009;182:799–816. https://doi.org/10.1111/j.1469-8137.2009.02846.x
• 8. Pinto E, Sigaud-kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P. Heavy metal-induced oxidative stress in algae. J Phycol. 2003;39:1008–1018. https://doi.org/10.1111/j.0022-3646.2003.02-193.x
• 9. Mallick N. Copper-induced oxidative stress in the chlorophycean microalga Chlorella vulgaris: response of the antioxidant system. J Plant Physiol. 2004;161:591–597. https://doi.org/10.1078/0176-1617-01230
• 10. Yruela I. Copper in plants: acquisition, transport and interactions. Funct Plant Biol. 2009;36:409–430. https://doi.org/10.1071/FP08288
• 11. Lu CM, Zhang JH. Copper-induced inhibition of PSII photochemistry in cyanobacterium Spirulina platensis is stimulated by light. J Plant Physiol. 1999;154:173– 178. https://doi.org/10.1016/S0176-1617(99)80206-5
• 12. Knauert S, Knauer K. The role of reactive oxygen species in copper toxicity to two freshwater green algae. J Phycol. 2008;44:311–319. https://doi.org/10.1111/j.1529-8817.2008.00471.x
• 13. Stanley RA. Toxicity of heavy metals and salts to Eurasian watermilfoil (Myriophyllum spicatum L.). Arch Environ Contam Toxicol. 1974;2:331–341. https://doi.org/10.1007/BF02047098
• 14. Wong MH, Bradshaw AD. Comparison of the toxicity of heavy metals, using root elongation of rye grass, Lolium perenne. New Phytol. 1982;91:255–261. https://doi.org/10.1111/j.1469-8137.1982.tb03310.x
• 15. Ince NH, Dirilgen N, Apikyan IG, Tezcanli G, Üstün B. Assessment of toxic interactions of heavy metals in binary mixtures: a statistical approach. Arch Environ Contam Toxicol. 1999;36:365–372. https://doi.org/10.1007/PL00006607
• 16. Macfie SM, Tarmohamed Y, Welbourn PM. Effects of cadmium, cobalt, copper, and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH. Arch Environ Contam Toxicol. 1994;24:454–458. https://doi.org/10.1007/BF00214835
• 17. Macfie SM, Welbourn PM. The cell wall as a barrier to uptake of metal ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae). Arch Environ Contam Toxicol. 2000;39:413–419. https://doi.org/10.1007/s002440010122
• 18. Mallick N, Rai LC. Physiological responses of non-vascular plants to heavy metals. In: Prasad MNV, Strzałka K, editors. Physiology and biochemistry of metal toxicity and tolerance in plants. Dordrecht: Springer; 2002. p. 111–147. https://doi.org/10.1007/978-94-017-2660-3_5
• 19. Lindberg S, Greger M. Plant genotypic differences under metal deficient and enriched conditions. In: Prasad MNV, Strzałka K, editors. Physiology and biochemistry of metal toxicity and tolerance in plants. Dordrecht: Springer; 2002. p. 357–393. https://doi.org/10.1007/978-94-017-2660-3_14
• 20. Hanikenne M. Chlamydomonas reinhardtii as a eukaryotic photosynthetic model for studies of heavy metal homeostasis and tolerance. New Phytol. 2003;159:331–340. https://doi.org/10.1046/j.1469-8137.2003.00788.x
• 21. Merchant S, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science. 2007;318:245–250. https://doi.org/10.1126/science.1143609
• 22. Luis P, Behnke K, Toepel J, Wilhelm C. Parallel analysis of transcript levels and physiological key parameters allows the identification of stress phase gene markers in Chlamydomonas reinhardtii under copper excess. Plant Cell Environ. 2006;29:2043–2054. https://doi.org/10.1111/j.1365-3040.2006.01579.x
• 23. Jamers A, Blust R, de Coen W, Griffin JL, Jones OAH. Copper toxicity in the microalga Chlamydomonas reinhardtii: an integrated approach. Biometals. 2013;26:731–740. https://doi.org/10.1007/s10534-013-9648-9
• 24. Prasad MNV, Drej K, Skawińska A, Strzałka K. Toxicity of cadmium and copper in Chlamydomonas reinhardtii wild-type (WT 2137) and cell wall deficient mutant strain (CW 15). Bull Environ Contam Toxicol. 1998;60:306–311. https://doi.org/10.1007/s001289900626
• 25. Fujiwara S, Kobayashi I, Hoshino S, Kaise T, Shimogawara K, Usuda H, et al. Isolation and characterization of arsenate-sensitive and resistant mutants of Chlamydomonas reinhardtii. Plant Cell Physiol. 2000;41:77–83. https://doi.org/10.1093/pcp/41.1.77
• 26. Collard JM, Matagne RF. Isolation and genetic analysis of Chlamydomonas reinhardtii strains resistant to cadmium. Appl Environ Microbiol. 1990;56:2051–2055.
• 27. Collard JM, Matagne RF. Cd2+ resistance in wild-type and mutant strains of Chlamydomonas reinhardtii. Environ Exp Bot. 1994;34:235–244. https://doi.org/10.1016/0098-8472(94)90044-2
• 28. Nagel K, Voigt J. In vitro evolution and preliminary characterization of a cadmium-resistant population of Chlamydomonas reinhardtii. Appl Environ Microbiol. 1989;55:526–528.
• 29. Davies DR, Plaskitt A. Genetical and structural analyses of cell-wall formation in Chlamydomonas reinhardi. Genet Res. 1971;17:33–43. https://doi.org/10.1017/S0016672300012015
• 30. Harris EH. The Chlamydomonas sourcebook. Amsterdam: Elsevier; 2009.
• 31. Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 1987;148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
• 32. Quinn GP, Keough MJ. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press; 2002. https://doi.org/10.1017/CBO9780511806384
• 33. Elena SF, Lenski RE. Microbial genetics: evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet. 2003;4:457–469. https://doi.org/10.1038/nrg1088
• 34. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. Experimental evolution. Trends Ecol Evol. 2012;27:547–560. https://doi.org/10.1016/j.tree.2012.06.001
• 35. Devars S, Hernández R, Moreno-Sánchez R. Enhanced heavy metal tolerance in two strains of photosynthetic Euglena gracilis by preexposure to mercury or cadmium. Arch Environ Contam Toxicol. 1998;34:128–135. https://doi.org/10.1007/s002449900296
• 36. Garcıa-Villada L, Rico M, Altamirano M, Sánchez-Martın L, López-Rodas V, Costas E. Occurrence of copper resistant mutants in the toxic cyanobacteria Microcystis aeruginosa: characterisation and future implications in the use of copper sulphate as algaecide. Water Res. 2004;38:2207–2213. https://doi.org/10.1016/j.watres.2004.01.036
• 37. Correa JA, Gonzalez P, Sanchez P, Munoz J, Orellana MC. Copper-algae interactions: inheritance or adaptation? Environmental Monitoring and Assesment. 1996;40(1):41–54. https://doi.org/10.1007/BF00395166
• 38. Nielsen HD, Brownlee C, Coelho SM, Brown MT. Inter-population differences in inherited copper tolerance involve photosynthetic adaptation and exclusion mechanisms in Fucus serratus. New Phytol. 2003;160:157–165. https://doi.org/10.1046/j.1469-8137.2003.00864.x
• 39. Bell G. Experimental genomics of fitness in yeast. Proc R Soc Lond B Biol Sci. 2010;277(1687):1459–1467. https://doi.org/10.1098/rspb.2009.2099
• 40. Finnegan EJ. Epialleles – a source of random variation in times of stress. Curr Opin Plant Biol. 2001;5(2):101–106. https://doi.org/10.1016/S1369-5266(02)00233-9
• 41. Mather, K. Polygenic inheritance and natural selection. Biol Rev. 1943;18:32–64. https://doi.org/10.1111/j.1469-185X.1943.tb00287.x
• 42. Rebound X, Bell G. Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity. 1997;78:507–514. https://doi.org/10.1038/hdy.1997.79
• 43. Lupi FM, Fernandes HML, Sá-Correia I. Increase of copper toxicity to growth of Chlorella vulgaris with increase of light intensity. Microb Ecol. 1998;35:193–198. https://doi.org/10.1007/s002489900074
• 44. Antal TK, Graevskaya EE, Matorin DN, Volgusheva AA, Osipov VA, Krendeleva TE, et al. Assessment of the effects of methylmercury and copper ions on primary processes of photosynthesis in green microalga Chlamydomonas moewusii by analysis of the kinetic curves of variable chlorophyll fluorescence. Biophysics. 2009;54:481–485. https://doi.org/10.1134/S0006350909040149
• 45. Devriese M, Tsakaloudi V, Garbayo I, León R, Vílchez C, Vigar J. Effect of heavy metals on nitrate assimilation in the eukaryotic microalga Chlamydomonas reinhardtii. Plant Physiol Biochem. 2001;39:443–448. https://doi.org/10.1016/S0981-9428(01)01257-8
• 46. Kučera T, Horáková H, Šonská A. Toxic metal ions in photoautotrophic organisms. Photosynthetica. 2008;46:481–489. https://doi.org/10.1007/s11099-008-0083-z
• 47. Hill KL, Hassett R, Kosman D, Merchant S. Regulated copper uptake in Chlamydomonas reinhardtii in response to copper availability. Plant Physiol. 1996;112:697–704. https://doi.org/10.1104/pp.112.2.697
• 48. Mendez-Alvarez S, Leisinger U, Eggen RIL. Adaptive responses in Chlamydomonas reinhardtii. International Microbiology. 1999;2:15–22.
• 49. Contreras-Porcia L, Dennett G, González A, Vergara E, Medina C, Correa JA, et al. Identification of copper-induced genes in the marine alga Ulva compressa (Chlorophyta). Mar Biotechnol. 2011;13:544–556. https://doi.org/10.1007/s10126-010-9325-8
• 50. Shah FUR, Ahmad N, Masood KR, Peralta-Videa JP, Ahmad FD. Heavy metal toxicity in plants. In: Ashraf M, Ozturk M, Ahmad MSA, editors. Plant adaptation and phytoremediation. Heidelberg: Springer; 2010. p. 71–97. https://doi.org/10.1007/978-90-481-9370-7_4
• 51. Arellano JB, Lázaro JJ, López-Gorgé J, Barón M. The donor side of photosystem II as the copper-inhibitory binding site. Photosynth Res. 1995;45:127–134. https://doi.org/10.1007/BF00032584
• 52. Burda K, Kruk J, Schmid GH, Strzałka K. Inhibition of oxygen evolution in photosystem II by Cu(II) ions is associated with oxidation of cytochrome b559. Biochem J. 2003;371:597–601. https://doi.org/10.1042/bj20021265
• 53. Liu S, Dong FQ, Yang CH, Tang CQ, Kuang TY. Reconstitution of photosystem II reaction center with Cu-chlorophyll a. J Integr Plant Biol. 2006;48:1330−1337. https://doi.org/10.1111/j.1744-7909.2006.00352.x
• 54. Nagalakshmi N, Prasad MNV. Copper-induced oxidative stress in Scenedesmus bijugatus: protective role of free radical scavengers. Bull Environ Contam Toxicol. 1998;61:623–628. https://doi.org/10.1007/s001289900806
• 55. Sandmann G. Böger P. Copper-mediated lipid peroxidation processes in photosynthetic membranes. Plant Physiol. 1980;66:797–800. https://doi.org/10.1104/pp.66.5.797
• 56. Stoiber TL, Shafer MM, Armstrong DE. Differential effects of copper and cadmium exposure on toxicity endpoints and gene expression in Chlamydomonas reinhardtii. Environ Toxicol Chem. 2010;29:191–200. https://doi.org/10.1002/etc.6
• 57. Peltier G, Thibault P. O2 uptake in the light in Chlamydomonas. Plant Physiol. 1985;79:225–230. https://doi.org/10.1104/pp.79.1.225
• 58. Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant. 2003;119:355–364. https://doi.org/10.1034/j.1399-3054.2003.00223.x
• 59. Lin YF, Aarts MGM. The molecular mechanism of zinc and cadmium stress response in plants. Cellular and Molecular Life Sciences. 2012;69:3187–3206. https://doi.org/10.1007/s00018-012-1089-z
• 60. Cuypers A, Keunen E, Bohler S, Jozefczak M, Opdenakker K, Gielen H, et al. Cadmium and copper stress induce a cellular oxidative challenge leading to damage versus signalling. In: Gupta DKG, Sandalios LM, editors. Metal toxicity in plants: perception, signaling and remediation. Berlin: Springer; 2011. p. 65–90.
• 61. Grzyb J, Waloszek A, Latowski D, Więckowski S. Effect of cadmium on ferredoxin: NADP+ oxidoreductase activity. J Inorg Biochem. 2004;98:1338–1346. https://doi.org/10.1016/j.jinorgbio.2004.04.004
• 62. Acan NL, Tezcan EF. Inhibition kinetics of sheep brain glutathione reductase by cadmium ion. Biochem Mol Med. 1995;54:33–37. https://doi.org/10.1006/bmme.1995.1005
• 63. Volland S, Schaumlöffel D, Dobritzsch D, Krauss GJ, Lütz-Mein U. Identification of phytochelatins in the cadmium-stressed conjugating green alga Micrasterias denticulata. Chemosphere. 2013;91:448–454. https://doi.org/10.1016/j.chemosphere.2012.11.064

Identyfikatory

DOI

10.5586/asbp.3569