Transcriptome sequencing (RNA-seq) analysis of the effects of metal nanoparticle exposure on the transcriptome of Chlamydomonas reinhardtii

Applied and Environmental Microbiology

Volumn 79, Issue 16, 2013, Pages 4774-4785

  Simon, Dana ^a   Domingos, Rute ^b   Hauser, Charles ^c   Hutchins, Colin ^a   Zerges, William ^d   Wilkinson, Kevin ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^c ST EDWARD'S UNIVERSITY   (United States)

^d Dept of Electrical and Computer Engineering   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; CHLAMYDOMONAS REINHARDTII; ELEVATED LEVEL; MULTIPLE MYELOMA; NANOPARTICLE (NPS); NANOPARTICLE EXPOSURES; TOXICOLOGICAL EFFECTS; TRANSCRIPTOMES;

CHEMOTHERAPY; ENCODING (SYMBOLS); RNA;

GENES;

BACTERIAL RNA; METAL NANOPARTICLE; QUANTUM DOT; TRANSCRIPTOME;

DATA ACQUISITION; DISEASE INCIDENCE; ENVIRONMENTAL CONDITIONS; EUKARYOTE; GENE EXPRESSION; GENETIC MARKER; GREEN ALGA; HEALTH CARE; PHOTOSYNTHESIS; POLLUTION EXPOSURE; RNA; TOXICOLOGY;

ARTICLE; CHLAMYDOMONAS REINHARDTII; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SEQUENCE ANALYSIS;

CHLAMYDOMONAS REINHARDTII; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METAL NANOPARTICLES; QUANTUM DOTS; RNA, BACTERIAL; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84880975812     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00998-13     Document Type: Article

References (70)

1. Chen L, Zhou L, Liu Y, Deng S, Wu H, Wang G. 2012. Toxicological effects of nanometer titanium dioxide (nano-TiO2) on Chlamydomonas reinhardtii. Ecotoxicol. Environ. Saf. 84:155-162.
2. Ivask A, Bondarenko O, Jepihhina N, Kahru A. 2010. Profiling of the reactive oxygen species-related ecotoxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Anal. Bioanal. Chem. 398:701-716.
3. Pujalté I, Passagne I, Brouillaud B, Tréguer M, Durand E, Ohayon-Courtés C, L'Azou B. 2011. Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part. Fibre Toxicol. 8:10-26.
4. Griffitt TJ, Weil R, Hyndman KA, Denslow ND, Powers K, Taylor D, Barber DS. 2007. Exposure to copper nanoparticles causes injury and acute lethality in zebrafish (Danio rerio). Environ. Sci. Technol. 41:8178-8186.
5. Nair PMG, Choi J. 2011. Characterization of a ribosomal protein L15 cDNA from Chironomus riparius (Diptera; Chironomidae): transcriptional regulation by cadmium and silver nanoparticles. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 159:157-162.
6. Chen M, Zhang M, Borlak J, Tong W. 2012. A decade of toxicogenomic research and its contribution to toxicological science. Toxicol. Sci. 130:217-228.
7. Wang Z, Gerstein M, Snyder M. 2009. RNA-seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10:57-63.
8. González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR. 2010. RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058-2084.
9. Miller R, Wu G, Deshpande RR, Vieler A, Gartner K, Li X, Moellering ER, Zäuner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo M-H, Hegg EL, Shachar-Hill Y, Shiu S-H, Benning C. 2010. Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154:1737-1752.
10. Maier T, Guell M, Serrano L. 2009. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583:3966-3973.
11. de Sousa Abreu R, Penalva LO, Marcotte E, Vogel C. 2009. Global signatures of protein and mRNA expression levels. Mol. Biosyst. 5:1512-1526.
12. Domingos RF, Simon DF, Hausser C, Wilkinson KJ. 2011. Bioaccumulation and effects of CdTe/CdS quantum dots on Chlamydomonas reinhardtii-nanoparticles or the free ions? Environ. Sci. Technol. 45:7664-7669.
13. Hutchins CM, Simon DF, Zerges W, Wilkinson KJ. 2010. Transcriptomic signatures in Chlamydomonas reinhardtii as Cd biomarkers in metal mixtures. Aquat. Toxicol. 100:120-127.
14. Jamers A, Blust R, Coen WD. 2009. Omics in algae: paving the way for a systems biological understanding of algal stress phenomena? Aquat. Toxicol. 92:114-121.
15. Simon DF, Descombes P, Zerges W, Wilkinson KJ. 2008. Global expression profiling of Chlamydomonas reinhardtii exposed to trace levels of free cadmium. Environ. Toxicol. Chem. 27:1668-1675.
16. Piccinno F, Gottschalk F, Seeger S, Nowack B. 2012. Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J. Nanopart. Res. 14:1109-1120.
17. Domingos RF, Tufenkji N, Wilkinson KJ. 2009. Aggregation of titanium dioxide nanoparticles: role of a fulvic acid. Environ. Sci. Technol. 43:1282-1286.
18. Domingos RF, Baalousha MA, Ju-Nam Y, Reid MM, Tufenkji N, Lead JR, Leppard GG, Wilkinson KJ. 2009. Characterizing manufactured nanoparticles in the environment: multimethod determination of particle sizes. Environ. Sci. Technol. 43:7277-7284.
19. Peulen TO, Wilkinson KJ. 2011. Diffusion of nanoparticles in a biofilm. Environ. Sci. Technol. 45:3367-3373.
20. Domingos RF, Franco C, Pinheiro JP. Stability of core/shell quantum dots-role of pH and small organic ligands. Environ. Sci. Pollut. Res. Int.,in press.
21. Carney RP, Kim JY, Qian H, Jin R, Mehenni H, Stellacci F, Bakr OM. 2011. Determination of nanoparticle size distribution together with density or molecular weight by 2D analytical ultracentrifugation. Nat. Commun. 2:335-342.
22. Elson EL, Magde D. 1974. Fluorescence correlation spectroscopy. I. Conceptual basis and theory. Biopolymers 13:1-27.
23. Balnois E, Papastavrou G, Wilkinson KJ. 2007. Force microscopy and force measurements of environmental colloids, p 405-467. In Wilkinson KJ, Lead J (ed), Environmental colloids: behaviour, structure and characterisation, vol 10. John Wiley & Sons, Ltd., Chichester, United Kingdom.
24. Harris ER. 1989. Culture and storage method in the Chlamydomonas sourcebook-a comprehensive guide to biology and laboratory use. Academic Press, San Diego, CA.
25. Kola H, Laglera LM, Parthasarathy N, Wilkinson KJ. 2004. Cadmium adsorption by Chlamydomonas reinhardtii and its interaction with the cell wall proteins. Environ. Chem. 1:172-179.
26. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu L-H, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Simon et al. Mittag M, et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245-251.
27. Li H, Ruan J, Durbin R. 2008. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18:1851-1858.
28. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106-R118. doi:10.1186/gb-2010-11-10-r106.
29. Bradford JR, Hey Y, Yates T, Li Y, Pepper SD, Miller CJ. 2010. A comparison of massively parallel nucleotide sequencing with oligonucleotide microarrays for global transcription profiling. BMC Genomics 11:282-294.
30. Young MD, Wakefield MJ, Smyth GK, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 11: R14-R26. doi:10.1186/gb-2010-11-2-r14.
31. Navarro E, Piccapetra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R. 2008. Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ. Sci. Technol. 42:8959-8964.
32. Franklin NM, Rogers NJ, Apte SC, Batley CE, Gadd GE, Casey PS. 2007. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ. Sci. Technol. 41:8484-8490.
33. Wang J, Zhang X, Chen Y, Sommerfeld M, Hu Q. 2008. Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. Chemosphere 73:1121-1128.
34. Domingos RF, Peyrot C, Wilkinson KJ. 2010. Aggregation of titanium dioxide nanoparticles: role of calcium and phosphate. Environ. Chem. 7:61-66.
35. Pasqui D, Golini L, Giovampaola CD, Atrei A, Barbucci R. 2011. Chemical and biological properties of polysaccharide-coated titania nanoparticles: the key role of proteins. Biomacromolecules 11:1243-1249.
36. Fatisson J, Quevedo IR, Wilkinson KJ, Tufenkji N. 2012. Physicochemical characterization of engineered nanoparticles under physiological conditions: effect of culture media components and particle surface coating. Colloids Surf. B Biointerfaces 91:198-204.
37. Wilkinson KJ, Buffle J. 2004. Critical evaluation of physicochemical parameters and processes for modeling the biological uptake of trace metals in environmental (aquatic) systems, p 445-533. In van Leeuwen H, Koester W (ed), Physicochemical kinetics and transport at chemicalbiological interphases. John Wiley & Sons Ltd., Chichester, United Kingdom.
38. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40:D109-D114. doi:10.1093/nar/gkr988.
39. Stolz A, Hilt W, Buchberger A, Wolf DH. 2011. Cdc48: a power machine in protein degradation. Trends Biochem. Sci. 36:515-523.
40. Castruita M, Casero D, Karpowicz SJ, Kropat J, Vieler A, Hsieh SI, Yan W, Cokus S, Loo JA, Benning C, Pellegrini M, Merchant SS. 2011. Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23:1273-1292.
41. Jamers A, Van der Ven K, Moens L, Robbens J, Potters G, Guisez U, Blust R, de Coen W. 2006. Effect of copper exposure on gene expression profiles in Chlamydomonas reinhardtii based on microarray analysis. Aquat. Toxicol. 80:249-260.
42. Sharma SS, Dietz K-J. 2008. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14:43-50.
43. Fischer BB, Krieger-Liszkay A, Eggen RIL. 2005. Oxidative stress induced by the photosensitizers neutral red (type I) or rose bengal (type II) in the light causes different molecular responses in Chlamydomonas reinhardtii. Plant Sci. 168:747-759.
44. Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324-332.
45. Eisele F, Schafer A, Wolf DH. 2010. Ubiquitylation in the ERAD pathway. Conjugation and deconjugation of ubiquitin family modifiers. Subcell. Biochem. 54:136-148.
46. Mou S, Zhang X, Ye N, Dong M, Liang C, Liang Q, Miao J, Xu D, Zheng Z. 2012. Cloning and expression analysis of two different LhcSR genes involved in stress adaptation in an Antarctic microalga, Chlamydomonas sp. ICE-L. Extremophiles 16:193-203.
47. Baba M, Suzuki I, Shiraiwa Y. 2011. Proteomic analysis of high-CO2-inducible extracellular proteins in the unicellular green alga, Chlamydomonas reinhardtii. Plant Cell Physiol. 52:1302-1314.
48. Harris EH. 2001. Chlamydomonas as a model organism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:363-406.
49. Tanaka A. 2007. Photosynthetic activity in winter needles of the evergreen tree Taxus cuspidata at low temperatures. Tree Physiol. 27:641-648.
50. + release from nanosilver. Talanta 105:15-19.
51. Bouldin JL, Ingle TM, Sengupta A, Alexander R, Hannigan RE, Buchanan RA. 2008. Aqueous toxicity and food chain transfer of quantum dots in freshwater algae and Ceriodaphnia dubia. Environ. Toxicol. Chem. 27:1958-1963.
52. Hanna J, Finley D. 2007. A proteasome for all occasions. FEBS Lett. 581:2854-2861.
53. Naujokat C, Fuchs D, Berges C. 2007. Adaptive modification and flexibility of the proteasome system in response to proteasome inhibition. Biochim. Biophys. Acta 1773:1389-1397.
54. Goldberg AL. 2012. Development of proteasome inhibitors as research tools and cancer drugs. J. Cell Biol. 199:583-588.
55. Verani CN. 2012. Metal complexes as inhibitors of the 26S proteasome in tumor cells. J. Inorg. Biochem. 106:59-67.
56. Yu X, Robinson JF, Sidhu JS, Hong S, Faustman EM. 2010. A systembased comparison of gene expression reveals alterations in oxidative stress, disruption of ubiquitin-proteasome system and altered cell cycle regulation after exposure to cadmium and methylmercury in mouse embryonic ibroblast. Toxicol. Sci. 114:356-377.
57. Forzani C, Lobréaux S, Mari S, Briat J-F, Lebrun N. 2002. Metal resistance in yeast mediated by the expression of a maize 20S proteasome alpha subunit. Gene 293:199-204.
58. Stoiber TL, Shafer MM, Armstrong DE. 22 July 2011. Induction of reactive oxygen species in Chlamydomonas reinhardtii in response to contrasting trace metal exposures. Environ. Toxicol. [Epub ahead of print.] doi:10.1002/tox.20743.
59. Burton NC, Guilarte TR. 2009. Manganese neurotoxicity: lessons learned from longitudinal studies in nonhuman primates. Environ. Health Perspect. 117:325-332.
60. Hegde AN, Upadhya SC. 2011. Role of ubiquitin-proteasome-mediated proteolysis in nervous system disease. Biochim. Biophys. Acta 1809:128-140.
61. Dohmen RJ, Willers I, Marques AJ. 2007. Biting the hand that feeds: Rpn4-dependent feedback regulation of proteasome function. Biochim. Biophys. Acta 1773:1599-1604.
62. Karpov DS, Osipov SA, Preobrazhenskaya OV, Karpov VL. 2008. Rpn4p is a positive and negative transcriptional regulator of the ubiquitinproteasome system. Mol. Biol. 42:456-462.
63. Karpov DS, Tyutyaeva VV, Beresten SF, Karpov VL. 2008. Mapping of the Rpn4p regions responsible for transcriptional activation of proteasome genes. Mol. Biol. 42:463-468.
64. Wang X, Xu H, Ha S-W, Ju D, Xie Y. 2010. Proteasomal degradation of Rpn4 in Saccharomyces cerevisiae is critical for cell viability under stressed conditions. Genetics 184:335-342.
65. Mannhaupt G, Schnall R, Karpov V, Vetter I, Feldmann H. 1999. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett. 450:27-34.
66. Leister D, Wang X, Haberer G, Mayer KFX, Kleine T. 2011. Intracompartmental and intercompartmental transcriptional networks coordinate the expression of genes for organellar functions. Plant Physiol. 157:386-404.
67. Teramoto H, Itoh T, Ono T-A. 2004. High-intensity-light-dependent and transient expression of new genes encoding distant relatives of lightharvesting chlorophyll-a/b proteins in Chlamydomonas reinhardtii. Plant Cell Physiol. 45:1221-1232.
68. Jung H-S, Chory J. 2010. Signaling between chloroplasts and the nucleus: can a system biology approach bring clarity to a complex and highly regulated pathway? Plant Physiol. 152:453-459.
69. Kleine T, Voigt C, Leister D. 2009. Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet. 25:185-192.
70. Domingos RF, Rafiei Z, Monteiro CE, Khan MAK, Wilkinson KJ. Agglomeration and dissolution of zinc oxide nanoparticles: role of pH, ionic strength and fulvic acid. Environ. Chem., in press.