Adaptation of microalgae to lindane: A new approach for bioremediation

Aquatic Toxicology

Volumn 109, Issue , 2012, Pages 25-32

  González, Raquel ^a   García Balboa, Camino ^a   Rouco, Mónica ^a   Lopez Rodas, Victoria ^a   Costas, Eduardo ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Adaptation; Bioremediation; Lindane; Microalgae; Mutation

Indexed keywords

FRESH WATER; LINDANE;

AQUATIC ECOSYSTEM; BIOACCUMULATION; BIOREMEDIATION; HCH; MICROALGA; PHYSIOLOGY; TOXICITY;

ACCLIMATIZATION; ARTICLE; BIOACCUMULATION; BIOREMEDIATION; CELL ACTIVITY; CELL CLONE; CELL GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYANOBACTERIUM; DICTYOSPHAERIUM CHLORELLOIDES; EVOLUTIONARY ADAPTATION; GREEN ALGA; GROWTH INHIBITION; MICROALGA; MICROCYSTIS AERUGINOSA; MUTATION RATE; NONHUMAN; PRIORITY JOURNAL; PSEUDOANABAENA LIMNETICA; SCENEDESMUS INTERMEDIUS; SENSITIVITY ANALYSIS; TOXICITY TESTING; WILD TYPE;

ADAPTATION, PHYSIOLOGICAL; BIODEGRADATION, ENVIRONMENTAL; CYANOBACTERIA; LINDANE; MICROALGAE; MUTATION; WATER POLLUTANTS, CHEMICAL;

CYANOBACTERIA;

EID: 84255209184     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.11.015     Document Type: Article

References (67)

1. Alexander M. Biodegradation and Bioremediation 1999, Academic Press, San Diego. second ed.
2. Arisoy M., Kolankaya N. Biodegradation of lindane by Pleurotus sajor-caju and toxic effects of lindane and its metabolites on mice. Bull. Environ. Contam. Toxicol. 1997, 59:352-359.
3. Asma V.M., Mathew K.J. Uptake of an organochlorine insecticide by a microalga Tetraselmis gracilis. Indian J. Fish. 2001, 48:49-53.
4. Baos R., Garcia-Villada L., Agrelo M., Lopez-Rodas V., Hiraldo F., Costas E. Short-term adaptation of microalgae in highly stressful environments: an experimental model analyzing the resistance of Scenedesmus intermedius (Chlorophyceae) to the heavy metals mixture from the Aznalcollar mine spill. Eur. J. Phycol. 2002, 37:593-600.
5. Belfiore N.M., Anderson S.L. Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat. Res. 2001, 489:97-122.
6. Benimelia C.S., Fuentesa M.S., Abatea C.M., Amorosoa M.J. Bioremediation of lindane-contaminated soil by Streptomyces sp. M7 and its effects on Zea mays growth. Int. Biodeterior. Biodegrad. 2008, 61:233-239.
7. British Standards Institute Precision of tests methods I. Guide for the determination of repeatability and reproductibility for a standard test method for inter-laboratory tests. BS 5497. Part I 1979, British Standards Institute, London.
8. Böltner D., Moreno-Morillas S., Ramos J.L. 16S rDNA phylogeny and distribution of lin genes in novel hexachlorocyclohexane-degrading Sphingomonas strains. Environ. Microbiol. 2005, 7:1329-1338.
9. Bradshaw A.D., Hardwick K. Evolution and stress-genotype and phenotype components. Biol. J. Linnean Soc. 1989, 37:137-155.
10. Breivik K., Pacyna J.M., Münch J. Use of alpha-, beta- and gamma-hexachlorocyclohexane in Europe, 1970-1996. Sci. Total Environ. 1999, 239:151-163.
11. Chaudhary P., Kumar M., Khangarot B.S., Kumar A. Degradation and detoxification of hexachlorocyclohexane isomers by Pseudomonas aeruginosa ITRC-5. Int. Biodeterior. Biodegrad. 2006, 57:107-113.
12. Costas E., Carrillo E., Ferrero L.M., Agrelo M., Garcia-Villada L., Juste J., Lopez-Rodas V. Mutation of algae from sensitivity to resistance against environmental selective agents: the ecological genetics of Dictyosphaerium chlorelloides (Chlorophyceae) under lethal doses of 3-(3,4-dichlorophenyl)-1,1-dimethylurea herbicide. Phycologia 2001, 40:391-398.
13. Costas E., Flores-Moya A., Perdigones N., Maneiro E., Blanco J.L., Garcia M.E., Lopez-Rodas V. How eukaryotic algae can adapt to Spain's Rio Tinto: a neo-Darwinian proposal for rapid adaptation to an extremely hostile ecosystem. New Phytol. 2007, 175:334-339.
14. Costas E., Flores-Moya A., Lopez-Rodas V. Rapid adaptation of algae to extreme environments (geothermal waters) by single mutation allows Noah's Arks for photosynthesizers during the Neoproterozoic snowball Earth?. New Phytol. 2008, 189:922-932.
15. Crow J.F., Kimura M. An introduction to population genetics theory 1970, Harper & Row, New York, NY, USA, p. 591.
16. El-Bestawy E.A., Abd El-Salam A.Z., Mansy A.E.H. Potential use of environmental cyanobacterial species in bioremedaition of lindane-contaminated effluents. Int. Biodeterior. Biodegrad. 2007, 59:180-192.
17. Falkowski P.G., Raven J.A. Aquatic photosynthesis 1997, Blackwell Scientific Publishers, Oxford, UK, p. 375.
18. Flores-Moya A., Costas E., Bañares-España E., García-Villada L., Altamirano M., Lopez-Rodas V. Adaptation of Spirogyra insignis (Chlorophyta) to an extreme natural environment (sulphureous waters) through pre-selective mutations. New Phytol. 2005, 166:655-661.
19. Fogg G.E. Algal adaptation to stress, some general remarks. Algal Adaptation to Environmental Stresses. Physiological, Biochemical and Molecular Mechanisms 2001, 1-20. Springer, Berlin, Germany. L.C. Rai, J.P. Gaur (Eds.).
20. Fragoeiro S., Magan N. Enzymatic activity, osmotic stress and degradation of pesticide mixtures in soil extract liquid broth inoculated with Phanerochaete chrysosporium and Trametes versicolor. Environ. Microbiol. 2005, 7:348-355.
21. Garcia-Villada L., Lopez-Rodas V., Bañares E., Flores-Moya A., Costas E. Evolution of microalgae in highly stressing environments: an experimental model analyzing the rapid adaptation of Dictyosphaerium chlorelloides (Chlorophyceae) from sensitivity to resistance against 2,4,6,-trinitrotoluene (TNT) by rare preselective mutation. J. Phycol. 2002, 38:1074-1081.
22. Garcia-Villada L., Rico M., Altamirano M., Sánchez L., Lopez-Rodas V., Costas E. Occurrence of copper resistant mutants in the toxic cyanobacteria Microcystis aeruginosa: characterization and future implications in the use of copper sulphate as algaecide. Water Res. 2004, 38:2207-2213.
23. Gupta A., Kaushik C.P., Kaushik A. Degradation of hexachlorocyclohexane (HCH; a, b, g and d) by Bacillus circulans and Bacillus brevis isolated from soil contaminated with HCH. Soil Biol. Biochem. 2000, 32:1803-1805.
24. Hansen P. Experiments on the accumulation of lindane ((-BCH) by the primary producers Chlorella spec. and Chlorella pyrenoidosa. Arch. Environm. Contam. Toxicol. 1979, 8:721-731.
25. Iannacone J., Gutiérrez A. Ecotoxicity of agrochemicals lindane and chlorpyrifos on the nematode Panagrellus, the microalgae Chlorella and the Allium-test. Agric. Técnica 1999, 59(2):85-95.
26. Junghans M., Backhaus T., Faust M., Scholze M., Grimmea L.H. Application and validation of approaches for the predictive hazard assessment of realistic pesticide mixtures. Aquat. Toxicol 2006, 76:93-110.
27. Kimura M., Maruyama T. The mutational load with epistatic gene interactions in fitness. Genetics 1966, 54:1337-1351.
28. Kirk J.T.O. Light and Photosynthesis in Aquatic Ecosystems 1994, Cambridge University Press, New York, NY, USA, p. 256. second ed.
29. Kobayashi H., Rittmann B.E. Microbial removal of hazardous organic compounds. Environ. Sci. Technol 1982, 16:170A-183A.
30. Kumar M., Chaudhary P., Dwivedi M., Kumar R., Paul D., Jain R.K., Garg S.K., Kumar A. Enhanced biodegradation of band d-hexachlorocyclohexane in the presence of a- and g-isomers in contaminated soils. Environ. Sci. Technol. 2005, 39:4005-4011.
31. Lal R., Pandey G., Sharma P., Kumari K., Malhotra S., Pandey R., Raina V., Kohler H.P.E., Holliger C., Jackson C., Oakeshott J.G. Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol. Mol. Biol. Rev. 2010, 74:58-80.
32. Li Y.F. Global technical hexachlorocyclohexane usage and its contamination consequences in the environment: from 1948 to 1997. Sci. Total Environ. 1999, 232:121-158.
33. Luria S., Delbrück M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 1943, 28:491-511.
34. Lopez-Rodas V., Agrelo M., Carrillo E., Ferrero L.M., Larrauri A., Martín-Otero L., Costas E. Resistance of microalgae to modern water contaminants as the result of rare spontaneous mutations. Eur. J. Phycol. 2001, 36:179-190.
35. Lopez-Rodas V., Flores-Moya A., Maneiro E., Perdigones N., Marva F., Garcia M.E., Costas E. Resistance to glyphosate in the cyanobacterium Microcystis aeruginosa as a result of preselective mutations. Evol. Ecol. 2007, 21:535-547.
36. Lopez-Rodas V., Marva F., Costas E., Flores-Moya A. Microalgal adaptation in the stressful acidic, metal-rich mine waters from Mynydd Parys (N Wales, UK) could be due to selection of preselective mutants. Environ. Exp. Bot. 2008, 61:43-48.
37. Lopez-Rodas V., Marva F., Rouco M., Costas E., Flores-Moya A. Adaptation of the chlorophycean Dictyosphaerium chlorelloides to the stressful acidic, mine metal-rich waters from Aguas Agrias Stream (SWSpain) as result of pre-selective mutations. Chemosphere 2008, 72:703-707.
38. Lopez-Rodas V., Carrera-Martinez D., Salgado E., Mateos-Sanz A., Baez J.C., Costas E. A fascinating example of microalgal adaptation to extreme crude oil contamination in a natural spill in Arroyo Minero, Río Negro, Argentina. An. Real Acad. Farm. 2009, 75:883-899.
39. Lopez-Rodas V., Perdigones N., Marva F., Maneiro E., Rouco M., Delgado A., Flores-Moya A., Costas E. Living in Vulcan's forge: algal adaptation to stressfull geothermal ponds on Vulcano Island (southern Italy) as result of pre-selective mutation. Phycol. Res. 2009, 57:111-117.
40. Macedo R.S., Lombardi A.T., Omachi C.Y., Rörig L.R. Effects of the herbicide bentazon on growth and photosystem II maximum quantum yield of the marine diatom Skeletonema costatum. Toxicol. In Vitro 2008, 22:716-722.
41. Manonmani H.K., Chandrashekariah D.H., Sreedhar Reddy N., Elecy C.D., Kunhi A.A.M. Isolation and acclimation of a microbial consortium for improved aerobic degradation of a-hexachlorocyclohexane. J. Agric. Food Chem. 2000, 48:4341-4351.
42. Miglioranza K.S.B., Sagrario M., Moreno J.E.A., Moreno V.J., Escalante A.H., Osterrieth M.L. Agricultural soil as a potential source of input of organochlorine pesticides into a nearby pond. Environ. Sci. Pollut. Res. 2002, 9:250-256.
43. Myers N., Knoll A.H. The biotic crisis and the future of evolution. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5389-5392.
44. Okeke B.C., Siddique T., Arbestain M.C., Frankenberger W.T. Biodegradation of g-hexachlorocyclohexane (lindane) and a-hexachlorocyclohexane in water and a soil slurry by a Padoraea species. J. Agric. Food Chem. 2002, 50:2548-2555.
45. Palumbi S.R. Human as world's greatest evolutionary force. Science 2001, 293:1786-1790.
46. Phillips T.M., Seech A.G., Lee H., Trevors J.T. Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation 2005, 16:363-392.
47. Franciskovic-Bilinski S., Bilinski H., Sirac S. Organic pollutants in stream sediments of Kupa River drainage basin. Fresenius Environ. Bull. 2005, 14:282-290.
48. Rigas F., Papadopoulou K., Dritsa V., Doulia D. Bioremediation of a soil contaminated by lindane utilizing the fungus Ganoderma australe via response surface methodology. J. Hazard. Mater. 2007, 140:325-332.
49. Sager R. Mendelian and non-mendelian inheritance of streptomycin resistance in Chlamydomonas. Proc. Natl. Acad. Sci. U.S.A. 1954, 40:356-363.
50. Sager R. Streptomycin as a mutagen for nonchromosomal genes. Proc. Natl. Acad. Sci. U.S.A 1962, 48:2018-2026.
51. Sager R. Genetic analysis of chloroplast DNA in Chlamydomonas. Adv. Genet. 1977, 19:287-340.
52. Sager R. Chloroplast genetics. Bioessays 1985, 3:180-184.
53. Semple K.T., Cain R.B., Schimdt S. Biodegradation of aromatic compounds by microalgae. FEMS Microbiol. Lett. 1999, 170:291-300.
54. Singh B.K., Kuhad R.C., Singh A., Tripathi K.K., Ghosh P.K. Microbial degradation of the pesticide lindane ((-hexachlorocyclohexane). Adv. Appl. Microbiol. 2000, 47:269-298.
55. Sniegowski P.D., Lenski R.E. Mutation and adaptation: the directed mutation controversy in evolutionary perspective. Ann. Rev. Ecol. Syst. 1995, 26:553-578.
56. Sniegowski P.D. Linking mutation to adaptation: overcoming stress at the spa. New Phytol. 2005, 166:360-362.
57. Spiess E.B. Genes in Populations 1989, John Wiley, New York, NY, USA. second ed.
58. Tanabe S., Subramanian A.N., Ramesh A., Kumaran P.L., Miyazaki N., Tatsukawa R. Persistent organochlorine residues in dolphins from the Bay of Benghal, south India. Mar. Pollut. Bull. 1993, 26:311-316.
59. Tao S., Xu F.L., Wang X.J., Liu W.X., Gong Z.M., Fang J.Y., Zhu L.Z., Luo Y.M. Organochlorine pesticides in agricultural soil and vegetables from Tianjin, China. Environ. Sci. Technol. 2005, 39:2494-2499.
60. Tejomyee S.B., Puranik P.R. Biodegradation of organochlorine pesticide, endosulfan, by a fungal soil isolate, Aspergillus niger. Int. Biodeterior. Biodegrad. 2007, 59:315-321.
61. Thomas J.C., Berger F., Jacquier M., Bernillon D., Baud-Grasset F., Truffaut N., Normand P., Vogel T.M., Simonet P. Isolation and characterization of a novel gamma-hexachlorocyclohexanedegrading bacterium. J. Bacteriol. 1996, 178:6049-6055.
62. van Eekert M.H., Van Ras N.J.P., Mentink G.H., Rijnaarts H.H.M., Stams A.J.M., Field J.A., Schraa G. Anaerobic transformation of b-hexachlorocyclohexane by methanogenic granular sludge and soil microflora. Environ. Sci. Technol. 1998, 32:3299-3304.
63. Thrusfield M. Veterinary Epidemiology 1995, Blackwell Science, New York.
64. Vijgen J., Yi L.F., Forter M., Lal R., Weber R. The legacy of lindane and technical HCH production. Organohalog. Compd. 2006, 68:899-904.
65. van Doesburg W., van Eekert M.H., Middeldorp P.J., Balk M., Schraa G., Stams A.J. Reductive dechlorination of beta-hexachlorocyclohexane (beta-HCH) by a Dehalobacter species in coculture with a Sedimentibacter sp. FEMS Microbiol. Ecol. 2005, 54:87-95.
66. Waliszewski S.M., Carvajal O., Infanzon R.M., Trujillo P., Aguirre A.A., Maxwell M. Levels of organochlorine pesticides in soils and rye plant tissues in a field study. J. Agric. Food Chem. 2004, 52:7045-7050.
67. Woodruff D.S. Declines of biomes and biotas and the future of evolution. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5471-5476.