Comparative transcriptome analysis uncovers roles of hydrogen sulfide for alleviating cadmium toxicity in Tetrahymena thermophila.
Cd stress
H2S
Oxidation resistance
Regulation of transport
Tetrahymena thermophila
Transcriptome
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
06 Jan 2021
06 Jan 2021
Historique:
received:
18
04
2020
accepted:
22
12
2020
entrez:
7
1
2021
pubmed:
8
1
2021
medline:
15
5
2021
Statut:
epublish
Résumé
Cadmium (Cd) is a nonessential heavy metal with potentially deleterious effects on different organisms. The organisms have evolved sophisticated defense system to alleviate heavy metal toxicity. Hydrogen sulfide (H The exposure of 30 μM Cd resulted in T. thermophila growth inhibition, cell nigrescence, and malondialdehyde (MDA) content considerably increase. However, exogenous NaHS (donor of H NaHS alleviated Cd stress mainly through inhibiting Cd absorbtion, promoting CdS nanoparticles formation, increasing oxidation resistance, and regulation of transport in free-living unicellular T. thermophila. These findings will expand our understanding for H
Sections du résumé
BACKGROUND
BACKGROUND
Cadmium (Cd) is a nonessential heavy metal with potentially deleterious effects on different organisms. The organisms have evolved sophisticated defense system to alleviate heavy metal toxicity. Hydrogen sulfide (H
RESULTS
RESULTS
The exposure of 30 μM Cd resulted in T. thermophila growth inhibition, cell nigrescence, and malondialdehyde (MDA) content considerably increase. However, exogenous NaHS (donor of H
CONCLUSION
CONCLUSIONS
NaHS alleviated Cd stress mainly through inhibiting Cd absorbtion, promoting CdS nanoparticles formation, increasing oxidation resistance, and regulation of transport in free-living unicellular T. thermophila. These findings will expand our understanding for H
Identifiants
pubmed: 33407108
doi: 10.1186/s12864-020-07337-9
pii: 10.1186/s12864-020-07337-9
pmc: PMC7788932
doi:
Substances chimiques
Cadmium
00BH33GNGH
Malondialdehyde
4Y8F71G49Q
Hydrogen Sulfide
YY9FVM7NSN
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
21Subventions
Organisme : National Natural Science Foundation of China
ID : Grant No. 31872224
Organisme : National Natural Science Foundation of China
ID : Grant No. 31471999
Organisme : Natural Science Foundation of Shanxi Province
ID : 201901D111008
Organisme : Natural Science Foundation of Shanxi Province
ID : 201801D221241
Références
Ahmad P, Ahanger MA, Egamberdieva D, Alam P, Alyemeni MN, Ashraf M. Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (hg) toxicity. J Plant Growth Regul. 2018;37:309–22.
Gupta AD, Karthikeyan S. Individual and combined toxic effect of nickel and chromium on biochemical constituents in E. coli using FTIR spectroscopy and principle component analysis. Ecotoxicol Environ Saf. 2016;130:289–94.
pubmed: 27152659
Jan S, Alyemeni MN, Wijaya L, Alam P, Siddique KH, Ahmad P. Interactive effect of 24-epibrassinolide and silicon alleviates cadmium stress via the modulation of antioxidant defense and glyoxalase systems and macronutrient content in Pisum sativum L. seedlings. BMC Plant Biol. 2018;18(1):146.
pubmed: 30012086
pmcid: 6048797
Saidi I, Ayouni M, Dhieb A, Chtourou Y, Chaïbi W, Djebali W. Oxidative damages induced by short-term exposure to cadmium in bean plants: protective role of salicylic acid. S Afr J Bot. 2013;85:32–8.
Khan MR, Nazir F, Asgher M, Per TS, Khan NA. Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol. 2015;173:9–18.
pubmed: 25462073
Zouari M, Elloumi N, Ahmed CB, Delmail D, Rouina BB, Abdallah FB, et al. Exogenous proline enhances growth, mineral uptake, antioxidant defense, and reduces cadmium-induced oxidative damage in young date palm (Phoenix dactylifera L.). Ecol Eng. 2016;86:202–9.
Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48(12):909–30.
pubmed: 20870416
Srikanth K, Pereira E, Duarte AC, Ahmad I. Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish—a review. Environ Sci Pollut Res Int. 2013;20(4):2133–49.
pubmed: 23334549
Kimura H. Production and physiological effects of hydrogen sulfide. Antioxid Redox Signal. 2014;20(5):783–93.
pubmed: 23581969
pmcid: 3910667
Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL. Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol. 2010;52(6):556–67.
pubmed: 20590986
Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, et al. Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem. 2013;65:67–74.
pubmed: 23416498
Zhang L, Pei Y, Wang H, Jin Z, Liu Z, Qiao Z, et al. Hydrogen sulfide alleviates cadmium-induced cell death through restraining ROS accumulation in roots of Brassica rapa L. ssp. pekinensis. Oxidative Med Cell Longev. 2015;2015:804603.
Mostofa MG, Rahman A, Ansary MM, Watanabe A, Fujita M, Tran LS. Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep. 2015;5:14078.
pubmed: 26361343
pmcid: 4566128
Gutiérrez JC, Amaro F, Martín-González A. From heavy metal-binders to biosensors: ciliate metallothioneins discussed. Bioessays. 2009;31(7):805–16.
pubmed: 19492353
Twagilimana L, Bohatier J, Groliere CA, Bonnemoy F, Sargos D. A new low-cost microbiotest with the protozoan Spirostomum teres: culture conditions and assessment of sensitivity of the ciliate to 14 pure chemicals. Ecotoxicol Environ Saf. 1998;41(3):231–44.
pubmed: 9799574
Gilron G, Gransden SG, Lynn DH, Broadfoot J, Scroggins R. A behavioral toxicity test using the ciliated protozoan Tetrahymena thermophila. I. Method description. Environ Toxicol Chem. 1999;18(8):1813–6.
Fu C, Xiong J, Miao W. Genome-wide identification and characterization of cytochrome P450 monooxygenase genes in the ciliate Tetrahymena thermophila. BMC Genomics. 2009;10:208.
pubmed: 19409101
pmcid: 2691746
Xiong J, Feng L, Yuan D, Fu C, Miao W. Genome-wide identification and evolution of ATP-binding cassette transporters in the ciliate Tetrahymena thermophila: a case of functional divergence in a multigene family. BMC Evol Biol. 2010;10:330.
pubmed: 20977778
pmcid: 2984421
Üstüntanır Dede AF, Arslanyolu M. Genome-wide analysis of the Tetrahymena thermophila glutathione S-transferase gene superfamily. Genomics. 2019;111(4):534–48.
pubmed: 30572113
Fu C, Yu T, Miao W, Shen Y. Tetrahymena: a good model organism for toxicology and ecotoxicology. Chin J Zool. 2005;40:108–13.
Somasundaram S, Abraham JS, Maurya S, Toteja R, Gupta R, Makhija S. Expression and molecular characterization of stress-responsive genes (hsp70 and Mn-sod) and evaluation of antioxidant enzymes (CAT and GPx) in heavy metal exposed freshwater ciliate, Tetmemena sp. Mol Biol Rep. 2019;46(5):4921–31.
pubmed: 31273612
Martín-González A, Díaz S, Borniquel S, Gallego A, Gutiérrez JC. Cytotoxicity and bioaccumulation of heavy metals by ciliated protozoa isolated from urban wastewater treatment plants. Res Microbiol. 2006;157(2):108–18.
pubmed: 16129584
Noever DA, Matsos HC, Looger LL. Bioconvective indicators in Tetrahymena: nickel and copper protection from cadmium poisoning. J Environ Sci Health, Part A: Environ Sci Eng. 1992;27(2):403–17.
Dayeh VR, Lynn DH, Bols NC. Cytotoxicity of metals common in mining effluent to rainbow trout cell lines and to the ciliated protozoan, Tetrahymena thermophila. Toxicol in Vitro. 2005;19(3):399–410.
pubmed: 15713547
Ali B, Gill RA, Yang S, Gill MB, Ali S, Rafiq MT, et al. Hydrogen sulfide alleviates cadmium-induced morpho-physiological and ultrastructural changes in Brassica napus. Ecotoxicol Environ Saf. 2014;110:197–207.
pubmed: 25255479
Jia H, Wang X, Dou Y, Liu D, Si W, Fang H, et al. Hydrogen sulfide-cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots. Sci Rep. 2016;6:39702.
pubmed: 28004782
pmcid: 5177925
Fu MM, Dawood M, Wang NH, Wu F. Exogenous hydrogen sulfide reduces cadmium uptake and alleviates cadmium toxicity in barley. J Plant Growth Regul. 2019;89:227–37.
Lv H, Xu J, Bo T, Wang W. Characterization of cystathionine β-synthase TtCbs1 and cysteine synthase TtCsa1 involved in cysteine biosynthesis in Tetrahymena thermophila. J Eukaryot Microbiol. 2020. https://doi.org/10.1111/jeu.12834 .
Yang L, Zeng J, Wang P, Zhu J. Sodium hydrosulfide alleviates cadmium toxicity by changing cadmium chemical forms and increasing the activities of antioxidant enzymes in Salix. Environ Exp Bot. 2018;156:161–9.
Krumov N, Oder S, Perner-Nochta I, Angelov A, Posten C. Accumulation of CdS nanoparticles by yeasts in a fed-batch bioprocess. J Biotechnol. 2007;132(4):481–6.
pubmed: 17900736
Juganson K, Mortimer M, Ivask A, Kasemets K, Kahru A. Extracellular conversion of silver ions into silver nanoparticles by protozoan Tetrahymena thermophila. Environ Sci Process Impacts. 2013;15(1):244–50.
pubmed: 24592441
Juganson K, Mortimer M, Ivask A, Pucciarelli S, Miceli C, Orupõld K, et al. Mechanisms of toxic action of silver nanoparticles in the protozoan Tetrahymena thermophila: from gene expression to phenotypic events. Environ Pollut. 2017;225:481–9.
pubmed: 28318795
Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11.
pubmed: 19289445
pmcid: 2672628
Chasapis CT, Andreini C, Georgiopolou AK, Stefanidou ME, Vlamis-Gardikas A. Identification of the zinc, copper and cadmium metalloproteome of the protozoon Tetrahymena thermophila by systematic bioinformatics. Arch Microbiol. 2017;199(8):1141–9.
pubmed: 28478602
Ogawa I, Nakanishi H, Mori S, Nishizawa NK. Time course analysis of gene regulation under cadmium stress in rice. Plant Soil. 2009;325:97–108.
Wang J, Lv Z, Lei Z, Chen Z, Lv B, Yang H, et al. Expression and functional analysis of cytochrome P450 genes in the wolf spider Pardosa pseudoannulata under cadmium stress. Ecotoxicol Environ Saf. 2019;172:19–25.
pubmed: 30669070
Armstrong RN. Glutathione S-transferases: reaction mechanism, structure, and function. Chem Res Toxicol. 1991;4(2):131–40.
pubmed: 1782341
García-Mata C, Lamattina L. Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol. 2010;188(4):977–84.
pubmed: 20831717
Toteja R, Makhija S, Sripoorna S, Abraham JS, Gupta R. Influence of copper and cadmium toxicity on antioxidant enzyme activity in freshwater ciliates. Indian J Exp Biol. 2017;55(10):694–701.
de Francisco P, Martin-Gonzalez A, Turkewitz AP, Gutierrez JC. Extreme metal adapted, knockout and knockdown strains reveal a coordinated gene expression among different Tetrahymena thermophila metallothionein isoforms. PLoS One. 2017;12(12):e0189076.
pubmed: 29206858
pmcid: 5716537
Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol. 2008;50(12):1518–29.
pubmed: 19093970
Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, et al. Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res Int. 2014;21(1):717–31.
pubmed: 23852465
Kim JS, Kim H, Yim B, Rhee JS, Won EJ, Lee YM. Identification and molecular characterization of two cu/Zn-SODs and Mn-SOD in the marine ciliate Euplotes crassus: modulation of enzyme activity and transcripts in response to copper and cadmium. Aquat Toxicol. 2018;199:296–304.
pubmed: 29605288
Xie ZZ, Liu Y, Bian JS. Hydrogen sulfide and cellular redox homeostasis. Oxidative Med Cell Longev. 2016;2016:6043038.
Zhang YY, Yang J, Yin XX, Yang SP, Zhu YG. Arsenate toxicity and stress responses in the freshwater ciliate Tetrahymena pyriformis. Eur J Protistol. 2012;48(3):227–36.
pubmed: 22342134
Zhang Y, Li Z, Kholodkevich S, Sharov A, Feng Y, Ren N, et al. Cadmium-induced oxidative stress, histopathology, and transcriptome changes in the hepatopancreas of freshwater crayfish (Procambarus clarkii). Sci Total Environ. 2019;666:944–55.
pubmed: 30970501
Díaz S, Amaro F, Rico D, Campos V, Benítez L, Martín-González A, et al. Tetrahymena metallothioneins fall into two discrete subfamilies. PLoS One. 2007;2(3):e291.
pubmed: 17356700
pmcid: 1808422
Viarengo A, Burlando B, Ceratto N, Panfoli I. Antioxidant role of metallothioneins: a comparative overview. Cell Mol Biol (Noisy-le-grand). 2000;46(2):407–17.
Rustichelli C, Visioli G, Kostecka D, Vurro E, di Toppi LS, Marmiroli N. Proteomic analysis in the lichen Physcia adscendens exposed to cadmium stress. Environ Pollut. 2008;156(3):1121–7.
pubmed: 18514371
Pocsi I, Prade RA, Penninckx MJ. Glutathione, altruistic metabolite in fungi. Adv Microb Physiol. 2004;49:1–76.
pubmed: 15518828
Zhang F, Li J, Huang J, Lin L, Wan X, Zhao J, et al. Transcriptome profiling reveals the important role of exogenous nitrogen in alleviating cadmium toxicity in poplar plants. J Plant Growth Regul. 2017;36:942–56.
Nair PM, Park SY, Choi J. Expression of catalase and glutathione S-transferase genes in Chironomus riparius on exposure to cadmium and nonylphenol. Comp Biochem Physiol C Toxicol Pharm. 2011;154(4):399–408.
Kim SH, Jung MY, Lee YM. Effect of heavy metals on the antioxidant enzymes in the marine ciliate Euplotes crassus. Toxicol Environ Heal Sci. 2011;3(4):213–9.
Pastore A, Federici G, Bertini E, Piemonte F. Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta. 2003;333(1):19–39.
pubmed: 12809732
Wang X, Wang C, Sheng H, Wang Y, Zeng J, Kang H, et al. Transcriptome-wide identification and expression analyses of ABC transporters in dwarf polish wheat under metal stresses. Biol Plant. 2017;61:293–304.
Bovet L, Feller U, Martinoia E. Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ Int. 2005;31(2):263–7.
pubmed: 15661293
Li ZS, Lu YP, Zhen RG, Szczypka M, Thiele DJ, Rea PA. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis (glutathionato) cadmium. PNAS. 1997;94(1):42–7.
pubmed: 8990158
McAleer MA, Breen MA, White NL, Matthews N. pABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells. J Biol Chem. 1999;274(33):23541–8.
pubmed: 10438534
Long Y, Li Q, Wang Y, Cui Z. MRP proteins as potential mediators of heavy metal resistance in zebrafish cells. Comp Biochem Physiol C Toxicol Pharmacol. 2011;153(3):310–7.
pubmed: 21147257
Ning Y, Dang H, Liu G, Xiong J, Yuan D, Feng L, et al. ATP-binding cassette transporter enhances tolerance to DDT in Tetrahymena. Sci China Life Sci. 2015;58(3):297–304.
pubmed: 25260902
Einicker-Lamas M, Morales MM, Miranda K, Garcia-Abreu J, Oliveira AJ, Silva FL, et al. P-glycoprotein-like protein contributes to cadmium resistance in Euglena gracilis. J Comp Physiol B. 2003;173(7):559–64.
pubmed: 12879347
Ivanina AV, Sokolova IM. Effects of cadmium exposure on expression and activity of P-glycoprotein in eastern oysters, Crassostrea virginica Gmelin. Aquat Toxicol. 2008;88(1):19–28.
pubmed: 18453012
Xu J, Tian H, Liu X, Wang W, Liang A. Localization and functional analysis of HmgB3p, a novel protein containing high-mobility-group-box domain from Tetrahymena thermophila. Gene. 2013;526(2):87–95.
pubmed: 23685281
Gaitonde MK. A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J. 1967;104(2):627–33.
pubmed: 6048802
pmcid: 1270629
Heath RL, Packer L. Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;125(1):189–98.
pubmed: 5655425
Peskin AV, Winterbourn CC. A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1). Clin Chim Acta. 2000;293(1–2):157–66.
pubmed: 10699430
Ozmen B, Ozmen D, Erkin E, Güner I, Habif S, Bayındır O. Lens superoxide dismutase and catalase activities in diabetic cataract. Clin Biochem. 2002;35(1):69–72.
pubmed: 11937081
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol. 2011;29(7):644–52.
pubmed: 21572440
pmcid: 21572440
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12:323.
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2007;36:D480–4.
pubmed: 18077471
pmcid: 2238879
Mao X, Cai T, Olyarchuk JG, Wei L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics. 2005;21(19):3787–93.
pubmed: 15817693
Larionov A, Krause A, Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinform. 2005;6:62.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2