Expression, Purification and Characterization of a Novel Rusticyanin from the Psychrotolerant Acidithiobacillus ferrivorans-CSCIED科技核心评价数据库-手机版

Expression, Purification and Characterization of a Novel Rusticyanin from the Psychrotolerant Acidithiobacillus ferrivorans

Expression, Purification and Characterization of a Novel Rusticyanin from the Psychrotolerant Acidithiobacillus ferrivorans

ES评分 0 浏览量：66 下载量：0

全文阅读下载引用收藏

DOI	doi.org/10.3390/separations10080448
刊名	Separations
年，卷(期)	2023, 10(8)
作者	Yuandong Liu*, Lixiang Chen, Xiangdong Shangguan, Jingying Ouyang, Jiayu He, Kan Wang, Yan Tong,Runlan Yu, Weimin Zeng, Xueling Wu, Li Shen,Guanzhou Qiu,
作者单位	中南大学
摘要	Rusticyanin plays a crucial role in ferrous oxidation of sulﬁde minerals during bioleaching for industrial metal extraction. Diverse isoforms of rusticyanin have been found, but until now, except for type-A rusticyanin, other isoforms or sources of rusticyanin have been scarcely investigated. Here, a rusticyanin (gene locus 0470) from the psychrophilic Acidithiobacillus ferrivorans was gene-cloned, expressed, puriﬁed, and assembled in vitro. All forms of the protein exhibit extreme acid stability, even at pH 0.3. The stability of the protein is obviously enhanced after binding of the copper cofactor; the oxidation state is more stable than the reduced state. The protein has characteristic UV-vis peaks and EPR signals similar to type-A or type-B rusticyanin but is different with a small position shift and an obvious intensity change. The vibrational spectrum of the apoprotein was more different than these between the oxidation and reduced states of the protein. The ferrous oxidation kinetic rate constant of the protein is obviously faster than that of both the type-A and type-B rusticyanins previously reported. Further bioinformatics analysis reveal their changes in sequence and molecule: the mutations related to the peculiar shield belt mostly account for the variation in the properties of the protein, and the classiﬁcation of the protein as a new isoform, type-C rusticyanin, is proposed.
Abstract	Rusticyanin plays a crucial role in ferrous oxidation of sulﬁde minerals during bioleaching for industrial metal extraction. Diverse isoforms of rusticyanin have been found, but until now, except for type-A rusticyanin, other isoforms or sources of rusticyanin have been scarcely investigated. Here, a rusticyanin (gene locus 0470) from the psychrophilic Acidithiobacillus ferrivorans was gene-cloned, expressed, puriﬁed, and assembled in vitro. All forms of the protein exhibit extreme acid stability, even at pH 0.3. The stability of the protein is obviously enhanced after binding of the copper cofactor; the oxidation state is more stable than the reduced state. The protein has characteristic UV-vis peaks and EPR signals similar to type-A or type-B rusticyanin but is different with a small position shift and an obvious intensity change. The vibrational spectrum of the apoprotein was more different than these between the oxidation and reduced states of the protein. The ferrous oxidation kinetic rate constant of the protein is obviously faster than that of both the type-A and type-B rusticyanins previously reported. Further bioinformatics analysis reveal their changes in sequence and molecule: the mutations related to the peculiar shield belt mostly account for the variation in the properties of the protein, and the classiﬁcation of the protein as a new isoform, type-C rusticyanin, is proposed.
关键词	rusticyanin; isoform; Acidithiobacillus ferrivorans; overexpression; characterization; kinetic rate constant
KeyWord	rusticyanin; isoform; Acidithiobacillus ferrivorans; overexpression; characterization; kinetic rate constant
基金项目
页码	1-16

参考文献
相关文献

Botuyan, M.V.; Toy-Palmer, A.; Chung, J.; Blake, R.C., 2nd; Beroza, P.; Case, D.A.; Dyson, H.J. NMR solution structure of Cu(I) rusticyanin from Thiobacillus ferrooxidans: Structural basis for the extreme acid stability and redox potential. J. Mol. Biol. 1996, 263, 752–767.
[Google Scholar]
[CrossRef]
[PubMed]

Valdes, J.; Pedroso, I.; Quatrini, R.; Dodson, R.J.; Tettelin, H.; Blake, R., II; Eisen, J.A.; Holmes, D.S. Acidithiobacillus ferrooxidans metabolism: From genome sequence to industrial applications. BMC Genom. 2008, 9, 597.
[Google Scholar]
[CrossRef]
[PubMed]

Wheaton, G.; Counts, J.; Mukherjee, A.; Kruh, J.; Kelly, R. The Confluence of Heavy Metal Biooxidation and Heavy Metal Resistance: Implications for Bioleaching by Extreme Thermoacidophiles. Minerals 2015, 5, 397–451.
[Google Scholar]
[CrossRef]

Cox, J.C.; Boxer, D.H. The purification and some properties of rusticyanin, a blue copper protein involved in iron(II) oxidation from Thiobacillus ferrooxidans. Biochem. J. 1978, 174, 497–502.
[Google Scholar]
[CrossRef]

Ronk, M.; Shively, J.E.; Shute, E.A.; Blake, R.C., 2nd. Amino acid sequence of the blue copper protein rusticyanin from Thiobacillus ferrooxidans. Biochemistry 1991, 30, 9435–9442.
[Google Scholar]
[CrossRef]

Yarzabal, A.; Appia-Ayme, C.; Ratouchniak, J.; Bonnefoy, V. Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 2004, 150, 2113–2123.
[Google Scholar]
[CrossRef]

Nunzi, F.; Guerlesquin, F.; Shepard, W.; Guigliarelli, B.; Bruschi, M. Active site geometry in the high oxido-reduction potential rusticyanin from Thiobacillus ferrooxidans. Biochem. Biophys. Res. Commun. 1994, 203, 1655–1662.
[Google Scholar]
[CrossRef]

Grossmann, J.G. The N-terminal extension of rusticyanin is not responsible for its acid stability. Biochemistry 2002, 41, 3619.
[Google Scholar]
[CrossRef]

Barrett, M.L. Atomic resolution crystal structures, EXAFS, and quantum chemical studies of rusticyanin and its two mutants provide insight into its unusual properties. Biochemistry 2006, 45, 2939.
[Google Scholar]
[CrossRef]

Yamada, T.; Hiraoka, Y.; Das Gupta, T.K.; Chakrabarty, A.M. Rusticyanin, a bacterial electron transfer protein, causes G(1) arrest in J774 and apoptosis in human cancer cells. Cell Cycle 2004, 3, 1182–1187.
[Google Scholar]
[CrossRef]

Cruz-Gallardo, I.; Diaz-Moreno, I.; Diaz-Quintana, A.; Donaire, A.; Velazquez-Campoy, A.; Curd, R.D.; Rangachari, K.; Birdsall, B.; Ramos, A.; Holder, A.A.; et al. Antimalarial Activity of Cupredoxins the Interaction of Plasmodium Merozoite Surface Protein 1(19) (MSP1(19)) and Rusticyanin. J. Biol. Chem. 2013, 288, 20896–20907.
[Google Scholar]
[CrossRef]
[PubMed]

Gonzalez-Arribas, E.; Falk, M.; Aleksejeva, O.; Bushnev, S.; Sebastian, P.; Feliu, J.M.; Shleev, S. A conventional symmetric biosupercapacitor based on rusticyanin modified gold electrodes. J. Electroanal. Chem. 2018, 816, 253–258.
[Google Scholar]
[CrossRef]

Sasaki, K. Respiratory isozyme, two types of rusticyanin of Acidithiobacillus ferrooxidans. Biosci. Biotechnol. Biochem. 2003, 67, 1047.
[Google Scholar]
[CrossRef]
[PubMed]

Ida, C. Kinetic rate constant for electron transfer between ferrous ions and novel Rusticyanin isoform in Acidithiobacillus ferrooxidans. J. Biosci. Bioeng. 2003, 95, 537.
[Google Scholar]
[CrossRef]

Hedrich, S.; Schloemann, M.; Johnson, D.B. The iron-oxidizing proteobacteria. Microbiology 2011, 157, 1551–1564.
[Google Scholar]
[CrossRef]

Ccorahua-Santo, R.; Eca, A.; Abanto, M.; Guerra, G.; Ramirez, P. Physiological and comparative genomic analysis of Acidithiobacillus ferrivorans PQ33 provides psychrotolerant fitness evidence for oxidation at low temperature. Res. Microbiol. 2017, 168, 482–492.
[Google Scholar]
[CrossRef]

Liljeqvist, M.; Valdes, J.; Holmes, D.S.; Dopson, M. Draft Genome of the Psychrotolerant Acidophile Acidithiobacillus ferrivorans SS3. J. Bacteriol. 2011, 193, 4304–4305.
[Google Scholar]
[CrossRef]

Jafarpour, R.; Fatemi, F.; Eidi, A.; Mehrnejad, F. Effect of the Met148Leu mutation on the structure and dynamics of the rusticyanin protein from Acidithiobacillus sp. FJ2. J. Biomol. Struct. Dyn. 2021, 39, 4122–4132.
[Google Scholar]
[CrossRef]

Panyushkina, A.E.; Babenko, V.V.; Nikitina, A.S.; Selezneva, O.V.; Tsaplina, I.A.; Letarova, M.A.; Kostryukova, E.S.; Letarov, A.V. Sulfobacillus thermotolerans: New insights into resistance and metabolic capacities of acidophilic chemolithotrophs. Sci. Rep. 2019, 9, 15069.
[Google Scholar]
[CrossRef]

Sousa, P.; Camacho, I.; Câmara, J.S.; Perestrelo, R. Urinary Proteomic/Peptidomic Biosignature of Breast Cancer Patients Using 1D SDS-PAGE Combined with Matrix-Assisted Laser Desorption/Ionization-Time of Flight Mass Spectrometry. Separations 2023, 10, 291.
[Google Scholar]
[CrossRef]

Zeng, J.; Geng, M.; Liu, Y.; Xia, L.; Liu, J.; Qiu, G. The sulfhydryl group of Cys 138 of rusticyanin from Acidithiobacillus ferrooxidans is crucial for copper binding. Biochim. Biophys. Acta-Proteins Proteom. 2007, 1774, 519–525.
[Google Scholar]
[CrossRef]
[PubMed]

Zeng, J.; Geng, M.; Liu, Y.; Zhao, W.; Xia, L.; Liu, J.; Qiu, G. Expression, purification and molecular modelling of the Iro protein from Acidithiobacillus ferrooxidans Fe-1. Protein Expr. Purif. 2007, 52, 146–152.
[Google Scholar]
[CrossRef]
[PubMed]

Bowers, K.; Markova, N. Value of DSC in Characterization and Optimization of Protein Stability. In Microcalorimetry of Biological Molecules: Methods and Protocols; Ennifar, E., Ed.; Methods in Molecular Biology; Humana Press: New York, NY, USA, 2019; Volume 1964, pp. 33–44.
[Google Scholar]

Wen, J.; Arthur, K.; Chemmalil, L.; Muzammil, S.; Gabrielson, J.; Jiang, Y. Applications of differential scanning calorimetry for thermal stability analysis of proteins: Qualification of DSC. J. Pharm. Sci. 2012, 101, 955–964.
[Google Scholar]
[CrossRef]

Feng, J.; Cai, H.; Wang, H.; Li, C.; Liu, S. Improved oxidative stability of fish oil emulsion by grafted ovalbumin-catechin conjugates. Food Chem. 2018, 241, 60–69.
[Google Scholar]
[CrossRef]

Brandes, N.; Welzel, P.B.; Werner, C.; Kroh, L.W. Adsorption-induced conformational changes of proteins onto ceramic particles: Differential scanning calorimetry and FTIR analysis. J. Colloid Interface Sci. 2006, 299, 56–69.
[Google Scholar]
[CrossRef]

Wu, T.; Jiang, Q.; Wu, D.; Hu, Y.; Chen, S.; Ding, T.; Ye, X.; Liu, D.; Chen, J. What is new in lysozyme research and its application in food industry? A review. Food Chem. 2019, 274, 698–709.
[Google Scholar]
[CrossRef]

Alderton, A.L.; Faustman, C.; Liebler, D.C.; Hill, D.W. Induction of redox instability of bovine myoglobin by adduction with 4-hydroxy-2-nonenal. Biochemistry 2003, 42, 4398–4405.
[Google Scholar]
[CrossRef]
[PubMed]

Sartor, G.; Mayer, E.; Johari, G.P. Calorimetric studies of the kinetic unfreezing of molecular motions in hydrated lysozyme, hemoglobin, and myoglobin. Biophys. J. 1994, 66, 249–258.
[Google Scholar]
[CrossRef]
[PubMed]
[Green Version]

Barth, A.; Zscherp, C. What vibrations tell us about proteins. Q. Rev. Biophys. 2002, 35, 369–430.
[Google Scholar]
[CrossRef]

Kyte, J.; Doolittle, R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157, 105–132.
[Google Scholar]
[CrossRef]

Gutfreund, H. Proteins: Structures and molecular properties (second edition). FEBS Lett. 1993, 323, 294.
[Google Scholar]
[CrossRef]

Ida, C.; Sasaki, K.; Ohmura, N.; Ando, A.; Saiki, H. Classification of rusticyanin structre genes from five different strains of Thiobacillus ferrooxidans into two groups. Process Metall. 1999, 9, 129–137.
[Google Scholar]
[CrossRef]

引用本文

Yuandong Liu*, Lixiang Chen, Xiangdong Shangguan, Jingying Ouyang, Jiayu He, Kan Wang, Yan Tong,Runlan Yu, Weimin Zeng, Xueling Wu, Li Shen,Guanzhou Qiu. Expression, Purification and Characterization of a Novel Rusticyanin from the Psychrotolerant Acidithiobacillus ferrivorans [J]. Separations. 2023; 10; (8). 1 - 16.

文献评论

相关学者

相关机构