Abstract
Heat shock proteins (HSPs) and HSP70-HSP90 organizing proteins (HOPs) are related, and they function together to maintain cellular homeostasis and respond to stress. In the present study, we reported the first molecular characteristics of HSP70 (designated as CeHSP70) and HOP (designated as CeHOP) genes from the freshwater green algae Closterium ehrenbergii and examined the changes in their expression profiles under heat stress and toxic chemicals treatment. CeHSP70 presented the conserved motif patterns and EEVD domain specific to cytosolic HSP70; CeHOP contained a typical domain of TPR repeats. Real-time PCR analysis showed that thermal stress considerably up-regulated both CeHOP and CeHSP70. In addition, the genes were significantly induced by CuCl2, CuSO4, and NiSO4, but not by K2Cr2O7, herbicide, and endocrine disrupting chemicals. These results suggest that CeHOP and CeHSP70 function together and play a role in responses to specific stressors and indicate their possible use as sensitive specific biomarkers in risk assessments.
References
Abassi S, Wang H, Ponmani T, Ki JS (2019) Small heat shock protein genes of the green algae Closterium ehrenbergii: cloning and differential expression under heat and heavy metal stresses. Environ Toxicol 34:1013–1024. https://doi.org/10.1002/tox.22772
Assimon VA, Southworth DR, Gestwicki JE (2015) Specific binding of tetratricopeptide repeat proteins to heat shock protein 70 (Hsp70) and heat shock protein 90 (Hsp90) is regulated by affinity and phosphorylation. Biochemistry 54:7120–7131. https://doi.org/10.1021/acs.biochem.5b00801
Baindur-Hudson S, Edkins AL, Blatch GL (2015) Hsp70/Hsp90 organising protein (Hop): beyond interactions with chaperones and prion proteins. Subcell Biochem 78:1–22. https://doi.org/10.1007/978-3-319-11731-7_3
Chankova S, Mitrovska Z, Miteva D et al (2013) Heat shock protein HSP70B as a marker for genotype resistance to environmental stress in Chlorella species from contrasting habitats. Gene 516:184–189. https://doi.org/10.1016/j.gene.2012.11.052
Ebenezer V, Ki J-S (2012) Evaluation of the sub-lethal toxicity of Cu, Pb, bisphenol A and polychlorinated biphenyl to the marine dinoflagellate Cochlodinium polykrikoides. Algae 27:63–70. https://doi.org/10.4490/algae.2012.27.1.063
Ebenezer V, Ki JS (2016) Toxic effects of Aroclor 1016 and bisphenol A on marine green algae Tetraselmis suecica, diatom Ditylum brightwellii and dinoflagellate Prorocentrum minimum. Korean J Microbiol 52:306–312. https://doi.org/10.7845/KJM.2016.6050
Guo R, Ki JS (2012) Differential transcription of heat shock protein 90 (HSP90) in the dinoflagellate Prorocentrum minimum by copper and endocrine-disrupting chemicals. Ecotoxicology 21:1448–1457. https://doi.org/10.1007/s10646-012-0898-z
Guo R, Ebenezer V, Ki JS (2012) Transcriptional responses of heat shock protein 70 (Hsp70) to thermal, bisphenol A, and copper stresses in the dinoflagellate Prorocentrum minimum. Chemosphere 89:512–520. https://doi.org/10.1016/j.chemosphere.2012.05.014
Guo R, Lee MA, Ki JS (2013) Different transcriptional responses of heat shock protein 70/90 in the marine diatom Ditylum brightwellii exposed to metal compounds and endocrine-disrupting chemicals. Chemosphere 92:535–543. https://doi.org/10.1016/j.chemosphere.2013.03.052
Guo R, Youn SH, Ki J-S (2015) Heat shock protein 70 and 90 genes in the harmful dinoflagellate Cochlodinium polykrikoides: genomic structures and transcriptional responses to environmental stresses. Int J Genomics 2015:1–12. https://doi.org/10.1155/2015/484626
Ichimura T, Kasai F (1984) Time lapse analyses of sexual reproduction in Closterium ehrenbergii (conjugatophyceae). J Phycol 20:258–265. https://doi.org/10.1111/j.0022-3646.1984.00258.x
Juneau P, Sumitomo H, Matsui S et al (2003) Use of chlorophyll fluorescence of Closterium ehrenbergii and Lemna gibba for toxic effect evaluation of sewage treatment plant effluent and its hydrophobic components. Ecotoxicol Environ Saf 55:1–8. https://doi.org/10.1016/s0147-6513(02)00130-6
Kim H, Wang H, Abassi S, Ki JS (2020) The herbicide alachlor severely affects photosystem function and photosynthetic gene expression in the marine dinoflagellate Prorocentrum minimum. J Environ Sci Health B Pestic Food Contam Agric Wastes 55:620–629. https://doi.org/10.1080/03601234.2020.1755198
Lamoth F, Juvvadi PR, Soderblom EJ et al (2015) Hsp70 and the cochaperone StiA (hop) orchestrate Hsp90-mediated caspofungin tolerance in Aspergillus fumigatus. Antimicrob Agents Chemother 59:4727–4733. https://doi.org/10.1128/AAC.00946-15
Lee MA, Guo R, Ebenezer V, Ki JS (2015) Evaluation and selection of reference genes for ecotoxicogenomic study of the green alga Closterium ehrenbergii using quantitative real-time PCR. Ecotoxicology 24:863–872. https://doi.org/10.1007/s10646-015-1430-z
Liu Y, Guan Y, Gao Q et al (2010) Cellular responses, biodegradation and bioaccumulation of endocrine disrupting chemicals in marine diatom Navicula incerta. Chemosphere 80:592–599. https://doi.org/10.1016/j.chemosphere.2010.03.042
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Morano KA (2007) New tricks for an old dog: the evolving world of Hsp70. Ann N Y Acad Sci 1113:1–14
Mosaviazam B, Ramezani A, Morowvat MH et al (2016) HSP70 gene expression analysis in Dunaliella salina under salt stress. Int J Pharmacogn Phytochem Res 8:767–770
Odunuga OO, Longshaw VM, Blatch GL (2004) Hop: more than an Hsp70/Hsp90 adaptor protein. BioEssays 26:1058–1068. https://doi.org/10.1002/bies.20107
Piano A, Valbonesi P, Fabbri E (2004) Expression of cytoprotective proteins, heat shock protein 70 and metallothioneins, in tissues of Ostrea edulis exposed to heat and heavy metals. Cell Stress Chaperones 9:134–142. https://doi.org/10.1379/483.1
Röhl A, Wengler D, Madl T et al (2015) Hsp90 regulates the dynamics of its cochaperone Sti1 and the transfer of Hsp70 between modules. Nat Commun 6:6655. https://doi.org/10.1038/ncomms7655
Rosic NN, Pernice M, Dove S et al (2011) Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chaperones 16:69–80. https://doi.org/10.1007/s12192-010-0222-x
Sathasivam R, Ebenezer V, Guo R, Ki JS (2016) Physiological and biochemical responses of the freshwater green algae Closterium ehrenbergii to the common disinfectant chlorine. Ecotoxicol Environ Saf 133:501–508. https://doi.org/10.1016/j.ecoenv.2016.08.004
Schmid AB, Lagleder S, Gräwert MA et al (2012) The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBO J 31:1506–1517. https://doi.org/10.1038/emboj.2011.472
Shao B, Zhu L, Dong M et al (2012) DNA damage and oxidative stress induced by endosulfan exposure in zebrafish (Danio rerio). Ecotoxicology 21:1533–1540. https://doi.org/10.1007/s10646-012-0907-2
Vayssier M, Le Guerhier F, Fabien JF et al (1999) Cloning and analysis of a Trichinella britovi gene encoding a cytoplasmic heat shock protein of 72 kDa. Parasitology 119:81–93. https://doi.org/10.1017/S0031182099004461
Wang H, Ki JS (2019) Molecular characterization and expression analysis of copper-zinc superoxide dismutases from the freshwater alga Closterium ehrenbergii under metal stress. Environ Toxicol 35:5–14. https://doi.org/10.1002/tox.22837
Wang H, Sathasivam R, Ki JS (2017) Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments. Algae 32:131–137. https://doi.org/10.4490/algae.2017.32.5.24
Wang H, Guo R, Ki JS (2018) 6.0 K microarray reveals differential transcriptomic responses in the dinoflagellate Prorocentrum minimum exposed to polychlorinated biphenyl (PCB). Chemosphere 195:398–409. https://doi.org/10.1016/j.chemosphere.2017.12.066
Watanebe S (2000) NIES-collection list of strains, 6th edn. National Institute for Environmental Studies Environment Agency Japan, Tsukuba
Wepener V, van Vuren JHJ, Chatiza FP et al (2005) Active biomonitoring in freshwater environments: early warning signals from biomarkers in assessing biological effects of diffuse sources of pollutants. Phys Chem Earth 30:751–761. https://doi.org/10.1016/j.pce.2005.08.018
Zhang Z, Quick MK, Kanelakis KC et al (2003) Characterization of a plant homolog of hop, a cochaperone of hsp90. Plant Physiol 131:525–535. https://doi.org/10.1104/pp.011940
Acknowledgements
We thank Dr. S. Kim at Environmental Bio Inc., Korea, for proving a cultured strain and Miss H. Kim for cell culture and microscopic observation.
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Abassi, S., Wang, H. & Ki, JS. Molecular cloning of heat shock protein 70 and HOP from the freshwater green algae Closterium ehrenbergii and their responses to stress. Cell Stress and Chaperones 25, 1117–1123 (2020). https://doi.org/10.1007/s12192-020-01143-8
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DOI: https://doi.org/10.1007/s12192-020-01143-8