Functional GFP-metallothionein fusion protein from Tetrahymena thermophila: A potential whole-cell biosensor for monitoring heavy metal pollution and a cell model to study metallothionein overproduction effects

BioMetals

Volumn 27, Issue 1, 2014, Pages 195-205

  Amaro, Francisco ^a   Turkewitz, Aaron P ^b   Martín González, Ana ^a   Gutiérrez, Juan Carlos ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Ciliate metallothioneins; GFP reporter; Heavy metals; Tetrahymena thermophila; Whole cell biosensor

Indexed keywords

CADMIUM; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; METALLOTHIONEIN; SOIL POLLUTANT;

ANALYSIS; CELL CULTURE; CYTOLOGY; GENETIC PROCEDURES; GENETICS; METABOLISM; SOIL POLLUTANT; TETRAHYMENA THERMOPHILA;

BIOSENSING TECHNIQUES; CADMIUM; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; METALLOTHIONEIN; RECOMBINANT FUSION PROTEINS; SOIL POLLUTANTS; TETRAHYMENA THERMOPHILA;

EID: 84893837733     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-014-9704-0     Document Type: Article

References (38)

1. Amaro F, Turkewitz AP, Martin-Gonzalez A, Gutierrez JC (2011) Whole-cell biosensors for detection of heavy metal ions in environmental samples based on metallothionein promoters from Tetrahymena thermophila. Microb Biotechnol 4:513-522
2. Aury JM, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM, Ségurens B, Daubin V, Anthouard V, Aiach N, Arnaiz O, Billaut A, Beisson J, Blanc I, Bouhouche K, Câmara F, Duharcourt S, Guigo R, Gogendeau D, Katinka M, Keller AM, Kissmehl R, Klotz C, Koll F, Le Mouël A, Lepère G, Malinsky S, Nowacki M, Nowak JK, Plattner H, Poulain J, Ruiz F, Serrano V, Zagulski M, Dessen P, Bétermier M, Weissenbach J, Scarpelli C, Schächter V, Sperling L, Meyer E, Cohen J, Wincker P (2006) Global trends of the whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171-178 (Pubitemid 44722053)
3. Belkin S (2003) Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 6:206-212 (Pubitemid 36841662)
4. Boldrin F, Santovito G, Formigari A, Bisharyan Y, Cassidy-Hanley D, Clark TG, Piccinni E (2008) MTT2, a copper-inducible metallothionein gene from Tetrahymena thermophila. Comp Biochem Physiol C 147:232-240 (Pubitemid 50010029)
5. Coppellotti O (1994) Effects of cadmium on Uronema marinum (Ciliophora, Scuticociliatida) from Antartica. Acta Protozool 33:159-167 (Pubitemid 2149772)
6. Cowan AT, Bowman GR, Edwards KF, Emerson JJ, Turkewitz AP (2005) Genetic, genomic and functional analysis of the granule lattice proteins in Tetrahymena secretory granules. Mol Biol Cell 16:4046-4060 (Pubitemid 41262877)
7. D′Souza SF (2001) Microbial biosensors. Biosens Bioelectron 49:337-353 (Pubitemid 32728156)
8. Dentler W (2000) Fixation of Tetrahymena cells for electron microscopy. In: Asai DJ, Forney JD (eds) Tetrahymena thermophila: methods in cell biology, vol 62. Academic Press, London, pp 323-331
9. Díaz S, Amaro F, Rico D, Campos V, Benitez L, Martin-Gonzalez A, Hamilton EP, Orias E, Gutierrez JC (2007) Tetrahymena metallothioneins fall into two discrete subfamilies. PLoS ONE 2:e291
10. Dunlop S, Chapman G (1981) Detoxification of zinc and cadmium by the freshwater protozoan Tetrahymena pyriformis. II Growth experiments and ultrastructural studies on sequestration of heavy metals. Environ Research 24:264-274 (Pubitemid 11080219)
11. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, Wortman JR, Badger JH, Ren Q, Amedeo P, Jones KM, Tallon LJ, Delcher AL, Salzberg SL, Silva JC, Haas BJ, Majoros WH, Farzad M, Carlton JM, Smith RK Jr, Garg J, Pearlman RE, Karrer KM, Sun L, Manning G, Elde NC, Turkewitz AP, Asai DJ, Wilkes DE, Wang Y, Cai H, Collins K, Stewart BA, Lee SR, Wilamowska K, Weinberg Z, Ruzzo WL, Wloga D, Gaertig J, Frankel J, Tsao CC, Gorovsky MA, Keeling PJ, Waller RF, Patron NJ, Cherry JM, Stover NA, Krieger CJ, del Toro C, Ryder HF, Williamson SC, Barbeau RA, Hamilton EP, Orias E (2006) Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4:c286 (Pubitemid 44379925)
12. Gaertig J, Gorovsky MA (1992) Efficient mass transformation of Tetrahymena thermophila by electroporation of conjugants. Proc Natl Acad Sci USA 89:9196-9200
13. Gallego A, Martin-Gonzalez A, Ortega R, Gutierrez JC (2007) Flow cytometry assessment of cytotoxicity and reactive oxygen species generation by single and binary mixtures of cadmium, zinc and copper on populations of the ciliated protozoan Tetrahymena thermophila. Chemosphere 68:647-661 (Pubitemid 46590295)
14. Gutierrez JC, Martin-Gonzalez A, Diaz S, Ortega R (2003) Ciliates as potential source of cellular and molecular biomarker/biosensors for heavy metal pollution. Eur J Protistol 39:461-467 (Pubitemid 38171077)
15. Gutierrez JC, Martin-Gonzalez A, Diaz S, Amaro F, Ortega R, Gallego A, Lucas MP (2008) Ciliates as cellular tools to study the eukaryotic cell-heavy metal interactions. In: Brown SE, Welton WC (eds) Heavy metal pollution. Nova Science Publishers, New York, pp 1-44
16. Gutierrez JC, Amaro F, Martin-Gonzalez A (2009) From heavy metal-binder to biosensors: ciliate metallothioneins discussed. BioEssays 31:805-816
17. Gutierrez JC, Amaro F, Diaz S, de Francisco P, Cubas LL, Martin-Gonzalez A (2011) Ciliate metallothioneins: unique microbial eukaryotic heavy-metal-binder molecules. J Biol Inorg Chem 16:1025-1034
18. Hakkila K, Maksimow M, Karp M, Virta M (2002) Reporter genes lucFF, luxCDABE, gfp and dsred have different characteristics in whole-cell bacterial sensors. Anal Biochem 301:235-242 (Pubitemid 34158188)
19. Hamilton EP, Orias E (2000) Genetically mapping new mutants and cloned genes. In: Asai DJ, Forney JD (eds) Tetrahymena thermophila: methods in cell biology, vol 62. Academic Press, London, pp 265-280
20. Keith LH, Telliard WA (1979) Priority pollutants: a perspective view. Environ Sci Technol 13:416-423
21. Kohlmeier S, Mancuso M, Tecon R, Harms H, van der Meer JR, Wells M (2007) Bioreporters: gfp versus lux revisited and single-cell response. Biosens Bioelectron 22:1578-1585 (Pubitemid 46185952)
22. Larionov A, Krause A, Miller W (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinform 6:62 (Pubitemid 41357953)
23. Lovley DR (2000) Environmental microbe-metal interactions. ASM Press, Washington DC
24. Magrisso S, Erel Y, Belkin S (2008) Microbial reporters of metal bioavailability. Microb Biotechnol 1:320-330
25. Martin-Gonzalez A, Diaz S, Borniquel S, Gallego A, Gutierrez JC (2006) Cytotoxicity and bioaccumulation of heavy metals by ciliated protozoa isolated from urban wastewater treatment plants. Res Microb 157:108-118 (Pubitemid 43243687)
26. Nassiri Y, Mansot JL, Wery J, Ginsburger-Vogel T, Amiard JC (1997) Ultrastructural and electron energy loss spectroscopy studies of sequestration mechanisms of Cd and Cu in the marine diatom Skeletonema costatum. Arch Environ Contam Toxicol 33:147-155 (Pubitemid 27415380)
27. Park M, Tsai S-L, Chen W (2013) Microbial biosensors: engineered microorganisms as the sensing machinery. Sensors 13:5777-5795
28. Piccinni E, Albergoni V (1996) Cadmium detoxification in Protists. Comp Biochem Physiol C 113C:141-147 (Pubitemid 26144778)
29. Pyne CK, Iftode F, Curgy J (1983) The effects of cadmium on the growth pattern and ultrastructure of the ciliate Tetrahymena thermophila. Biol Cel 48:121-132
30. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
31. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, Gaertig J, Gorovsky MA (2002) A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc Natl Acad Sci USA 97:3734-3739 (Pubitemid 34252175)
32. Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509-544 (Pubitemid 28411137)
33. Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161-1208 (Pubitemid 40655271)
34. van der Meer JR, Belkin S (2010) Where microbiology meets microengineering: design and applications of reporter bacteria. Nat Rev Microb 8:511-522
35. van der Meer JR, Tropel D, Jasper M (2004) Illuminating the detection chain of bacterial bioreporters. Environ Microbiol 6:1005-1020 (Pubitemid 39275255)
36. Visviki I, Rachlin JW (1994) Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects on growth. Arch Environ Contam Toxicol 26:149-153 (Pubitemid 24175467)
37. Walmsley RM, Keenan P (2000) The eukaryote alternative: advantages of using yeasts in place of bacteria in microbial biosensor development. Biotechnol Bioprocess Eng 5:387-394
38. Yao M-C, Yao C-H (1991) Transformation of Tetrahymena to cycloheximide resistance with a ribosomal protein gene through sequence replacement. Proc Natl Acad Sci USA 88:9493-9497 (Pubitemid 21915657)