Stress responses and metal tolerance of Chlamydomonas acidophila in metal-enriched lake water and artificial medium

Extremophiles

Volumn 11, Issue 4, 2007, Pages 551-562

  Spijkerman, Elly ^a   Barua, Deepak ^a,b   Gerloff Elias, Antje ^a   Kern, Jürgen ^c   Gaedke, Ursula ^a   Heckathorn, Scott A ^b  

^a UNIVERSITY OF POTSDAM   (Germany)

^b UNIVERSITY OF TOLEDO   (United States)

^c LEIBNIZ INSTITUTE FOR AGRICULTURAL ENGINEERING AND BIOECONOMY ATB   (Germany)

Author keywords

Chlamydomonas acidophila; Heat shock protein accumulation; Lake water incubation; Metal accumulation; Metal stress; Photosynthetic yield

Indexed keywords

CHAPERONIN; FRESH WATER; HEAT SHOCK PROTEIN 70; IRON; PHOSPHORUS; SMALL HEAT SHOCK PROTEIN; ZINC;

ADAPTATION; ANIMAL; ARTICLE; CHEMICALLY INDUCED DISORDER; CHEMISTRY; CHLAMYDOMONAS; CULTURE MEDIUM; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOPHYSIOLOGY; PH; PHOTOSYNTHESIS; PHOTOSYSTEM II; STRESS; TIME; TRANSPORT AT THE CELLULAR LEVEL; WATER POLLUTANT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL TRANSPORT; CHAPERONIN 60; CHLAMYDOMONAS; CULTURE MEDIA; FRESH WATER; HEAT-SHOCK PROTEINS, SMALL; HSP70 HEAT-SHOCK PROTEINS; HYDROGEN-ION CONCENTRATION; IRON; PHOSPHORUS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; STRESS; TIME FACTORS; WATER POLLUTANTS, CHEMICAL; ZINC;

ALGAE; CHLAMYDOMONAS; CHLAMYDOMONAS ACIDOPHILA;

EID: 34347343852     PISSN: 14310651     EISSN: 14334909     Source Type: Journal    
DOI: 10.1007/s00792-007-0067-0     Document Type: Article

References (71)

1. Barua D, Heckathorn SA (2006) The interactive effects of light and temperature on heat-shock protein accumulation in Solidago altissima (Asteraceae) in the field and laboratory. Am J Bot 93:102-109
2. Bates SS, Tessier A, Campbell PGC, Buffle J (1982) Zinc adsorption and transport by Chlamydomonas variabilis and Scenedesmus subspicatus (Chlorophyceae) grown in semicontinuous culture. J Phycol 18:521-529
3. Bissinger V, Jander J, Tittel J (2000) A new medium free of organic carbon to cultivate organisms from extremely acidic mining lakes (pH 2.7). Acta Hydrochim Hydrobiol 28:310-312
4. Borbely G, Suranyi G, Kos P (1990) Stress responses of cyanobacteria and the pleiotropic effects of light deprivation. FEMS Microbiol Ecol 74:141-152
5. Bringezu K, Lichtenberger O, Leopold I, Neumann D (1999) Heavy metal tolerance of Silene vulgaris. J Plant Physiol 154:536-546
6. Doi H, Kikuchi E, Shikano S (2001) Carbon and nitrogen stable isotope ratios analysis of food sources for Chironomus acerbiphilus larvae (Diptera Chironomidae) in strongly acidic lake Katanuma. Radioisotopes 50:601-611
7. Downs CA, Ryan SL, Heckathorn SA (1999) The chloroplast small heat-shock protein: evidence for a general role in protecting photosystem II against oxidative stress and photoinhibition. J Plant Physiol 155:488-496
8. Drzymalla C, Schroda M, Beck CF (1996) Light-inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol Biol 31:1185-1194
9. Endo T, Asada K (1996) Dark induction of the non-photochemical quenching of chlorophyll fluorescence by acetate in Chlamydomonas reinhardtii. Plant Cell Physiol 37:551-555
10. Friese K, Hupfer M, Schultze M (1998) Chemical characteristics of water and sediment in acid mining lakes of the Lusatian lignite district. In: Geller W, Klapper H, Salomons W (eds) Acidic mining lakes: acid mine drainage, limnology and reclamation. Springer, Berlin, pp 25-45
11. Gaur JP, Rai LC (2001) Heavy metal tolerance in algae. In: Rai LC, Gaur JP (eds) Algal adaptation to environmental stresses-physiological, biochemical and molecular mechanisms. Springer, Varanasi, India, pp 363-388
12. Gerloff-Elias A, Spijkerman E, Pröschold T (2005a) Effect of external pH on the growth, photosynthesis and photosynthetic electron transport of Chlamydomonas acidophila Negoro, isolated from an extremely acidic lake (pH 2.6). Plant Cell Environ 28:1218-1229
13. Gerloff-Elias A, Spijkerman E, Schubert H (2005b) Light acclimation of Chlamydomonas acidophila accumulating in the hypolimnion of an acidic lake (pH 2.6). Freshw Biol 50:1301-1314
14. Gerloff-Elias A, Barua D, Mölich A, Spijkerman E (2006) Temperature- and pH-dependent accumulation of heat-shock proteins in the acidophilic green alga Chlamydomonas acidophila. FEMS Microbiol Ecol 56:345-354
15. Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr 543:137-145
16. Gimmler H (2001) Acidophilic and acidotolerant algae. In: Rai LC, Gaur JP (eds) Algal adaptation to environmental stresses. Physioloigcal, biochemical and molecular mechanisms. Springer, Varanasi, India, pp 259-290
17. Graham JM, Arancibia-Avila P, Graham LE (1996) Effects of pH and selected metals on growth of the filamentous green alga Mougeotia under acidic conditions. Limnol Oceanogr 41:263-270
18. Gyure RA, Konopka A, Brooks A, Doemel W (1987) Algal and bacterial activities in acidic (pH3) strip mine lakes. Appl Environ Microb 53:2069-2076
19. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1-11
20. Hallberg EM, Shu YM, Hallberg RL (1993) Loss of mitochondrial Hsp60 function: non-equivalent effects on matrix-targeted and intermembrane-targeted proteins. Mol Cell Biol 13:3050-3057
21. Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126:1266-1274
22. Harrison GI, Campbell PGC, Tessier A (1986) Effects of pH changes on zinc uptake by Chlamydomonas variabilis grown in batch culture. Can J Fish Aquat Sci 43:687-693
23. Heckathorn SA, Ryan SL, Baylis JA, Wang DF, Hamilton EW, Cundiff L, Luthe DS (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct Plant Biol 29:933-944
24. Heckathorn SA, Mueller JK, LaGuidice S, Zhu B, Barrett T, Blair B, Dong Y (2004) Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. Am J Bot 91:1312-1318
25. Heyde M, Portalier R (1990) Acid shock proteins of Escherichia coli. FEMS Microbiol Lett 69:19-26
26. 2+. Plant Cell Physiol 46:729-735
27. Ivorra N, Kraak MHS, Admiraal W (1995) Use of lake water in testing copper toxicity to desmid species. Water Res 29:2113-2117
28. Ivorra N, Barranguet C, Jonker M, Kraak MHS, Admiraal W (2002) Metal-induced tolerance in the freshwater microbenthic diatom Gomphonema parvulum. Environ Pollut 116:147-157
29. 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191-194
30. Kromkamp JC, Domin A, Dubinsky Z, Lehmann C, Schanz F (2001) Changes in photosynthetic properties measured by oxygen evolution and variable chlorophyll fluorescence in a simulated entrainment experiment with the cyanobacterium Planktothrix rubescens. Aquat Sci 63:363-382
31. Krupa Z, Baszynski T (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus- direct and indirect effects on light and dark reactions. Acta Physiol Plant 17:177-190
32. Laksanalamai P, Robb FT (2004) Small heat shock proteins from extremophiles: a review. Extremophiles 8:1-11
33. Lessmann D, Deneke R, Ender R, Hemm M, Kapfer M, Krumbeck H, Wollmann K, Nixdorf B (1999) Lake Plessa 107 (Lusatia, Germany)-an extremely acidic shallow mining lake. Hydrobiologia 408:293-299
34. Lessmann D, Fyson A, Nixdorf B (2000) Phytoplankton of the extremely acidic mining lakes of Lusatia (Germany) with pH < 3. Hydrobiologia 433:123-128
35. Lewis S, Donkin ME, Depledge MH (2001) Hsp70 expression in Enteromorpha intestinalis (Chlorophyta) exposed to environmental stressors. Aquat Toxicol 51:277-291
36. Lin CY, Chen YM, Key JL (1985) Solute leakage in soybean seedlings under various heat shock regimes. Plant Cell Physiol 26:1493-1498
37. Ma M, Zhu W, Wang Z, Witkamp GJ (2003) Accumulation, assimilation and growth inhibition of copper on freshwater alga (Scenedesmus subspicatus 86.81 SAG) in the presence of EDTA and fulvic acid. Aquat Toxicol 63:221-228
38. Mann H, Fyfe WS (1989) Metal uptake and Fe-oxide, Ti-oxide biomineralization by acidophilic microorganisms in mine-waste environments, Elliot Lake, Canada. Can J Earth Sci 26:2731-2735
39. Mann H, Tazaki K, Fyfe WS, Beveridge TJ, Humphrey R (1987) Cellular lepidocrocite precipitation and heavy-metal sorption in Euglena sp. (unicellular alga): Implications for biomineralization. Chem Geol 63:39-43
40. Nalewajko C, Colman B, Olaveson M (1997) Effects of pH on growth, photosynthesis, respiration, and copper tolerance of three Scenedesmus strains. Environ Exp Bot 37:153-160
41. Neumann D, Lichtenberger O, Gunther D, Tschiersch K, Nover L (1994) Heat-shock proteins induce heavy-metal tolerance in higher plants. Planta 194:360-367
42. 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
43. Nishikawa K, Tominaga N (2001) Isolation, growth, ultrastructure, and metal tolerance of the green alga, Chlamydomonas acidophila (Chlorophyta). Biosci Biotechnol Biochem 65:2650-2656
44. Nishikawa K, Yamakoshi Y, Uemura I, Tominaga N (2003) Ultrastructural changes in Chlamydomonas acidophila (Chlorophyta) induced by heavy metals and polyphosphate metabolism. FEMS Microbiol Ecol 44:253-259
45. Nixdorf B, Mischke U, Lessmann D (1998) Chrysophytes and chlamydomonads: pioneer colonists in extremely acidic mining lakes (pH < 3) in Lusatia (Germany). Hydrobiologia 370:315-327
46. Nixdorf B, Krumbeck H, Jander J, Beulker C (2003) Comparison of bacterial and phytoplankton productivity in extremely acidic mining lakes and eutrophic hard water lakes. Acta Oecol 24:281-288
47. Olaveson MM, Stokes PM (1989) Responses of the acidophilic alga Euglena mutabilis (Euglenophyceae) to carbon enrichment at pH 3. J Phycol 25:529-539
48. Packroff G (2000) Protozooplankton in acidic mining lakes with special respect to ciliates. Hydrobiologia 433:157-166
49. Panaretou B, Piper PW (1992) The plasma membrane of yeast acquires a novel heat shock protein (hsp30) and displays a decline in proton pumping ATPase levels in response to both heat-shock and the entry to stationary phase. Eur J Biochem 206:635-640
50. Parkhill JP, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517-529
51. 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
52. Poskuta JW, Parys E, Romanowska E (1996) Toxicity of lead to photosynthesis, accumulation of chlorophyll, respiration and growth of Chlorella pyrenoidosa. Protective role of dark respiration. Acta Physiol Plant 18:165-171
53. Pyza E, Mak P, Kramarz P, Laskowski R (1997) Heat shock proteins (HSP70) as biomarkers in ecotoxicological studies. Ecotoxicol Environ Saf 38:244-251
54. Ralph PJ, Burchett MD (1998) Photosynthetic response of Halophila ovalis to heavy metal stress. Environ Pollut 103:91-101
55. Schroda M, Vallon O, Wollman FA, Beck CF (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell 11:1165-1178
56. Schroda M, Vallon O, Whitelegge JP, Beck CF, Wollman FA (2001) The chloroplastic GrpE homolog of Chlamydomonas: two isoforms generated by differential splicing. The Plant Cell 13:2823-2839
57. Schuster G, Even D, Kloppstech K, Ohad I (1988) Evidence for protection by heat-shock proteins against photoinhibition during heat-shock. EMBO J 7:1-6
58. Shaked Y, Kustka AB, Morel FMM (2005) A general kinetic model for iron acquisition by eukaryotic phytoplankton. Limnol Oceanogr 50:872-882
59. Simmons JA, Long JM, Ray JW (2004) What limits the productivity of acid mine drainage treatment ponds? Mine Water Environ 23:44-53
60. 2 evolution in Anacystis nidulans. Plant Physiol 83:12-14
61. Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025-1037
62. Spijkerman E, Garcia-Mendoza E, Matthijs HCP, van Hunnik E, Coesel PFM (2004) Negative effects of P-buffering and pH on photosynthetic activity of planktonic desmid species. Photosynthetica 42:49-57
63. Tanaka Y, Nishiyama Y, Murata N (2000) Acclimation of the photosynthetic machinery to high temperature in Chlamydomonas reinhardtii requires synthesis de novo of proteins encoded by the nuclear and chloroplast genomes. Plant Physiol 124:441-449
64. Varotto C, Maiwald D, Pesaresi P, Jahns P, Salamini F, Leister D (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J 31:589-599
65. Vigneault B, Campbell PGC (2005) Uptake of cadmium by freshwater green algae: effects of pH and aquatic humic substances. J Phycol 41:55-61
66. Vigneault B, Percot A, Lafleur M, Campbell PGC (2000) Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances. Environ Sci Technol 34:3907-3913
67. de Vos CHR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853-858
68. Whitton BA (1970) Toxicity of heavy metals to freshwater algae: a review. Phykos 9:116-125
69. Woelfl S, Whitton BA (2000) Sampling, preservation and quantification of biological samples from highly acidic environments (pH <= 3). Hydrobiologia 433:173-180
70. Woelfl S, Tittel J, Zippel B, Kringel R (2000) Occurrence of an algal mass development in an acidic (pH 2.5), iron and aluminium-rich coal mining pond. Acta Hydrochim Hydrobiol 28:305-309
71. Wollgiehn R, Neumann D (1999) Metal stress response and tolerance of cultured cells from Silene vulgaris and Lycopersicon peruvianum: Role of heat stress proteins. J Plant Physiol 154:547-553