Abstract
Euglena mutabilis is a protist ubiquitously found in extreme environments such as acid mine drainages which are often rich in arsenic. The response of E. mutabilis to this metalloid was compared to that of Euglena gracilis, a protist not found in such environments. Membrane fatty acid composition, cell surface properties, arsenic accumulation kinetics, and intracellular arsenic speciation were determined. The results revealed a modification in fatty acid composition leading to an increased membrane fluidity in both Euglena species under sublethal arsenic concentrations exposure. This increased membrane fluidity correlated to an induced gliding motility observed in E. mutabilis in the presence of this metalloid but did not affect the flagellar dependent motility of E. gracilis. Moreover, when compared to E. gracilis, E. mutabilis showed highly hydrophobic cell surface properties and a higher tolerance to water-soluble arsenical compounds but not to hydrophobic ones. Finally, E. mutabilis showed a lower accumulation of total arsenic in the intracellular compartment and an absence of arsenic methylated species in contrast to E. gracilis. Taken together, our results revealed the existence of a specific arsenical response of E. mutabilis that may play a role in its hypertolerance to this toxic metalloid.
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Akter KF, Owens G, Davey DE, Naidu R (2006) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol 184:97–149
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Aposhian HV (1997) Enzymatic methylation of arsenic species and other new approaches to arsenic toxicity. Annu Rev Pharmacol Toxicol 317:397–419
Bertin PN, Heinrich-Salmeron A, Pelletier E, Goulhen-Chollet F, Arsène-Ploetze F, Gallien S, Lauga B, Casiot C, Calteau A, Vallenet D, Bonnefoy V, Bruneel O, Chane-Woon-Ming B, Cleiss-Arnold J, Duran R, Elbaz-Poulichet F, Fonknechten N, Giloteaux L, Halter D, Koechler S, Marchal M, Mornico D, Schaeffer C, Smith AAT, Van Dorsselaer A, Weissenbach J, Médigue C, Le Paslier D (2011) Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics. ISME J. doi:10.1038/ismej.2011.51
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Bluemlein K, Raab A, Feldmann J (2009) Stability of arsenic peptides in plant extracts: off-line versus on-line parallel elemental and molecular mass spectrometric detection for liquid chromatographic separation. Anal Bioanal Chem 393:357–366
Bluemlein K, Raab A, Meharg AA, Charnock JM, Feldmann J (2008) Can we trust mass spectrometry for determination of arsenic peptides in plants: comparison of LC-ICP-MS and LC-ES-MS/ICP-MS with XANES/EXAFS in analysis of Thunbergia alata. Anal Bioanal Chem 390:1739–1751
Brake SS, Dannelly HK, Connors KA (2001) Controls on the nature and distribution of an alga in coal mine-waste environments and its potential impact on water quality. Environ Geol 40:458–469
Bray JP, Broady PA, Niyogi DK, Harding JS (2008) Periphyton communities in New Zealand streams impacted by acid mine drainage. Mar Freshwat Res 59:1084–1091
Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personné JC (2006) Diversity of microorganisms in Fe-As-rich acid mine drainage waters of Carnoulès, France. Appl Environ Microbiol 72:551–556
Casiot C, Bruneel O, Personné JC, Leblanc M, Elbaz-Poulichet F (2004) Arsenic oxidation and bioaccumulation by the acidophilic protozoan, Euglena mutabilis, in acid mine drainage (Carnoulès, France). Sci Total Environ 320:259–267
Casiot C, Egal M, Elbaz-Poulichet F, Bruneel O, Bancon-Montigny C, Cordier MA, Gomez E, Aliaume C (2009) Hydrological and geochemical control of metals and arsenic in a Mediterranean river contaminated by acid mine drainage (the Amous River, France); preliminary assessment of impacts on fish (Leuciscus cephalus). Appl Geochem 24:787–799
Casiot C, Morin G, Juillot F, Bruneel O, Personné JC, Leblanc M, Duquesne K, Bonnefoy V, Elbaz-Poulichet F (2003) Bacterial immobilization and oxidation of arsenic in acid mine drainage (Carnoulès creek, France). Water Res 37:2929–2936
Egal M, Casiot C, Morin G, Elbaz-Poulichet F, Cordier MA, Bruneel O (2010) An updated insight into the natural attenuation of As concentrations in Reigous Creek (southern France). Appl Geochem 25(12):1949–1957
Einicker-Lamas M, Soares MJ, Soares MS, Oliveira MM (1996) Effects of cadmium on Euglena gracilis membrane lipids. Braz J Med Biol Res 29:941–948
Heipieper HJ, Isken S, Saliola M (2000) Ethanol tolerance and membrane fatty acid adaptation in adh multiple and null mutants of Kluyveromyces lactis. Res Microbiol 151:777–784
Kordialik-Bogacka E (2011) Surface properties of yeast cells during heavy metal biosorption. Cent Eur J Chem 9:348–351
Miot J, Morin G, Skouri-Panet F, Férard C, Aubry E, Briand J, Wang Y, Ona-Nguema G, Guyot F, Brown GE (2008) XAS study of arsenic coordination in Euglena gracilis exposed to arsenite. Environ Sci Technol 42:5342–5347
Miot J, Morin G, Skouri-Panet F, Férard C, Poitevin A, Aubry E, Ona-Nguema G, Juillot F, Guyot F, Brown GE Jr (2009) Speciation of arsenic in Euglena gracilis cells exposed to As(V). Environ Sci Technol 43:3315–3321
Morrison WR, Smith LM (1964) Preparation of fatty acid methyl esters and dimethylacetate from lipids with boron fluoride–methanol. J Lipid Res 5:600608
Nichols P, Stulp BK, Jones JG, White DC (1986) Comparison of fatty acid content and DNA homology of the filamentous gliding bacteria Vitreoscilla, Flexibacter, Filibacter. Arch Microbiol 146:1–6
Olaveson MM, Nalewajko C (2000) Effects of acidity on the growth of two Euglena species. Hydrobiologia 433:39–56
Olaveson MM, Stokes PM (1989) Responses of the acidophilic alga Euglena mutabilis (Euglenophyceae) to carbon enrichment at pH 3. J Phycol 25:529–539
Pawlik-Skowronska B, Pirszel J, Kalinowska R, Skowronski T (2004) Arsenic availability, toxicity and direct role of GSH and phytochelatins in As detoxification in the green alga Stichococcus bacillaris. Aquat Toxicol 70:201–212
Pepi M, Heipieper HJ, Fischer J, Ruta M, Volterrani M, Focardi SE (2008) Membrane fatty acids adaptive profile in the simultaneous presence of arsenic and toluene in Bacillus sp. ORAs2 and Pseudomonas sp. ORAs5 strains. Extremophiles 12:343–349
Qin J, Lehr CR, Yuan C, Le XC, McDermott TR, Rosen BP (2009) Biotransformation of arsenic by a yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci U S A 106:5213–5217
Raab A, Feldmann J, Meharg AA (2004) The nature of arsenic–phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134:1113–1122
Raab A, Schat H, Meharg AA, Feldmann J (2005) Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annuus): formation of arsenic–phytochelatin complexes during exposure to high arsenic concentrations. New Phytol 168:551–558
Rocchetta I, Mazzuca M, Conforti V, Ruiz L, Balzaretti V, De Molina MDCR (2006) Effect of chromium on the fatty acid composition of two strains of Euglena gracilis. Environ Pollut 141:353–358
Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33
Scanlan PD, Marchesi JR (2008) Micro-eukaryotic diversity of the human distal gut microbiota: qualitative assessment using culture-dependent and -independent analysis of faeces. ISME J 2:1183–1193
Stallwitz E, Hader DP (1994) Effects of heavy metals on motility and gravitactic orientation of the flagellate, Euglena gracilis. Eur J Protistol 30:18–24
Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotechnol 20:659–667
Valente TM, Gomes CL (2007) The role of two acidophilic algae as ecological indicators of acid mine drainage sites. J Iberian Geol 33:283–294
Wolowski K, Turnau K, Henriques FS (2008) The algal flora of an extremely acidic, metal-rich drainage pond of Sao Domingos pyrite mine (Portugal). Cryptogam Algol 29:313–324
Acknowledgments
The study was financed by the ANR 07-BLANC-0118 project (Agence Nationale de la Recherche). David Halter was supported by a grant from the French Ministry of Education and Research. This work was performed within the framework of the research network “Arsenic Metabolism in Micro-organisms” (GDR2909-CNRS).
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Halter, D., Casiot, C., Heipieper, H.J. et al. Surface properties and intracellular speciation revealed an original adaptive mechanism to arsenic in the acid mine drainage bio-indicator Euglena mutabilis . Appl Microbiol Biotechnol 93, 1735–1744 (2012). https://doi.org/10.1007/s00253-011-3493-y
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DOI: https://doi.org/10.1007/s00253-011-3493-y