Synthesis of intracellular cobalt ferrite nanocrystals by extreme acidophilic archaea Ferroplasma thermophilum

Abstract

Ferroplasma thermophilum, a sort of extreme acidophilic archaea, which can synthesize intracellular cobalt ferrite nanocrystals, is investigated in this study. The nanocrystals were analyzed with ultrathin sections and transmission electron microscope, with the size of 20–60 nm, the number of more than 30 in each cell at average, which indicated that F. thermophilum can synthesize intracellular nanocrystals and also belongs to high-yield nanocrystals-producing strain. Intriguingly, the nanocrystals contain ferrite and cobalt characterized by EDS X-ray analysis, suggesting that both cobalt and ferrite are potentially contributed to the formation of nanocrystals. Moreover, under the different energy source culture conditions of FeSO₄ and CuFeS₂, the size and the morphology of the nanocrystals are different. It was also found that the higher initial Fe availability leads to an induced synthesis of larger nanocrystals and the lower oxidation-reduction potential (ORP) leads to an induced effect on the synthesis of nanocrystals with abnormal unhomogeneous size, which suggested that the higher initial Fe availability and the lower oxidation-reduction potential lead to a higher uptake efficiency of iron ions of F. thermophilum by iron and ORP gradient culture.

References

[1] QinW-q, YangC-r, LaiS-s, WangJ, LiuK, ZhangBo. Bioleaching of chalcopyrite by moderately thermophilic microorganisms [J]. Bioresource Technology, 2013, 129: 200

[2] ZhaoH-b, WangJ, YangC-r, HuM-h, GanX-w, TaoL, QinW-q, QiuG-zhou. Effect of redox potential on bioleaching of chalcopyrite by moderately thermophilic bacteria: An emphasis on solution compositions [J]. Hydrometallurgy, 2015, 151141

[3] ZhaoH-b, WangJ, HuM-h, QinW-q, ZhangY-s, QiuG-zhou. Synergistic bioleaching of chalcopyrite and bornite in the presence of Acidithiobacillus ferrooxidans [J]. Bioresource Technology, 2013, 14971-76

[4] ZhaoH-b, WangJ, GanX-w, HuM-h, ZhangE-x, QinW-q, QiuG-zhou. Cooperative bioleaching of chalcopyrite and silver-bearing tailing by mixed moderately thermophilic culture: An emphasis on the chalcopyrite dissolution with XPS and electrochemical analysis [J]. Minerals Engineering, 2015, 81: 29

[5] WuS-f, YangC-r, QinW-q, JiaoF, WangJ, ZhangY-sheng. Sulfur composition on surface of chalcopyrite during its bioleaching at 50 °C [J]. Transactions of Nonferrous Metals Society of China, 2015, 25(25): 12-4110

[6] YangB-j, ZhaoC-x, LuoW, LiaoR, GanM, WangJ, LiuX-d, QiuG-zhou. Catalytic effect of silver on copper release from chalcopyrite mediated by Acidithiobacillus ferrooxidans [J]. Journal of Hazardous Materials, 2020, 392122290

[7] ChangK-x, ZhangY-s, ZhangJ-m, LiT-f, WangJ, QinW-qing. Effect of temperature-induced phase transitions on bioleaching of chalcopyrite [J]. Transactions of Nonferrous Metals Society of China, 2019, 29(29): 10-2183

[8] WuA-x, HuK-j, WangH-j, ZhangA-q, YangYing. Effect of ultraviolet mutagenesis on heterotrophic strain mutation and bioleaching of low grade copper ore [J]. Journal of Central South University, 2017, 24(24): 10-2245

[9] ZhaoH-b, WangJ, QinW-q, HuM-h, ZhuS, QiuG-zhou. Electrochemical dissolution process of chalcopyrite in the presence of mesophilic microorganisms [J]. Minerals Engineering, 2015, 71159

[10] ZhaoH-b, WangJ, QinW-q, ZhengX-h, TaoL, GanX-w, QiuG-zhou. Surface species of chalcopyrite during bioleaching by moderately thermophilic bacteria [J]. Transactions of Nonferrous Metals Society of China, 2015, 25(25): 8-2725

[11] ZhaoH-b, HuM-h, LiY-n, ZhuS, QinW-q, QiuG-z, WangJun. Comparison of electrochemical dissolution of chalcopyrite and bornite in acid culture medium [J]. Transactions of Nonferrous Metals Society of China, 2015, 25(25): 1-303

[12] NancucheoI, JohnsonD B. Production of glycolic acid by Chemolithotrophic iron- and sulfur-oxidizing bacteria and its role in delineating and sustaining acidophilic sulfide mineral-oxidizing consortia [J]. Applied and Environmental Microbiology, 2010, 76(76): 2-461

[13] WangX-x, LiaoR, ZhaoH-b, HongM-x, HuangX-t, PengH, WenW, QinW-q, QiuG-z, HuangC-m, WangJun. Synergetic effect of pyrite on strengthening bornite bioleaching by Leptospirillum ferriphilum [J]. Hydrometallurgy, 2018, 1769

[14] LiuS, XieL, LiuJ, LiuG-y, ZhongH, WangY-x, ZengH-bo. Probing the interactions of hydroxamic acid and mineral surfaces: Molecular mechanism underlying the selective separation [J]. Chemical Engineering Journal, 2019, 374123

[15] ZhaoH-b, HuangX-t, WangJ, LiY-n, LiaoR, WangX-x, QiuX, XiongY-m, QinW-q, QiuG-zhou. Comparison of bioleaching and dissolution process of p-type and n-type chalcopyrite [J]. Minerals Engineering, 2017, 109153

[16] YangB-j, LinM, FangJ-h, ZhangR-y, LuoW, WangX-x, LiaoR, WuB-q, WangJ, GanM, LiuB, ZhangY, LiuX-d, QinW-q, QiuG-zhou. Combined effects of jarosite and visible light on chalcopyrite dissolution mediated by Acidithiobacillus ferrooxidans [J]. Science of the Total Environment, 2020, 698134175

[17] QinW-q, LiuK, DiaoM-x, WangJ, ZhangY-s, YangC-r, JiaoFen. Oxidation of arsenite (As(III)) by ferric iron in the presence of pyrite and a mixed moderately thermophilic culture [J]. Hydrometallurgy, 2013, 13753-59

[18] LefevreC T, BazylinskiD A. Ecology, diversity, and evolution of magnetotactic bacteria [J]. Microbiology and Molecular Biology Reviews, 2013, 77(77): 3-497

[19] UebeR, SchuelerD. Magnetosome biogenesis in magnetotactic bacteria [J]. Nature Reviews Microbiology, 2016, 14(10): 621-637

[20] FaivreD, MenguyN, PosfaiM, SchuelerD. Environmental parameters affect the physical properties of fast-growing magnetosomes [J]. American Mineralogist, 2008, 93(23): 463-469

[21] PosfaiM, LefevreT, TrubitsynD, BazylinskiA, FrankelB. Phylogenetic significance of composition and crystal morphology of magnetosome minerals [J]. Frontiers in Microbiology, 2013, 4: 344

[22] LeaoP, TeixeiraS, CyprianoJ, FarinaM, AbreuF, BazylinskiA, LinsU. North-seeking magnetotactic gammaproteobacteria in the southern hemisphere [J]. Applied and Environmental Microbiology, 2016, 82(82): 18-5595

[23] JiB-y, ZhangS-d, ZhangW-j, RouyZ, AlbertoF, SantiniC, MangenotS, GagnotS, PhilippeN, PradelN, ZhangL-c, TempelS, LiY, MedigueC, HenrissatB, CoutinhoP M, BarbeV, TallaE, WuL-fei. The chimeric nature of the genomes of marine magnetotactic coccoid-ovoid bacteria defines a novel group of Proteobacteria [J]. Environmental Microbiology, 2017, 19(19): 3-1103

[24] Huizar-FelixA M, MunozD, OrueI, MagenC, IbarraA, BarandiaranJ M, MuelaA, Fdez-GubiedaM L. Assemblies of magnetite nanoparticles extracted from magnetotactic bacteria: A magnetic study [J]. Applied Physics Letters, 2016, 108(6): 0631096

[25] BazylinskiD A, FrankelR B, HeywoodB R, MannS, KingJ W, DonaghayP L, HansonA K. Controlled biomineralization of magnetite (Fe304) and greigite (Fe₃S₄) in a magnetotactic bacterium [J]. Applied and Environmental Microbiology, 1995, 61619-3232

[26] LefevreC T, MenguyN, AbreuF, LinsU, PosfaiM, ProzorovT, PignolD, FrankelR B, BazylinskiD A. A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria [J]. Science, 2011, 334(334): 6063-1720

[27] Barber-ZuckerS, ZarivachR. A look into the biochemistry of magnetosome biosynthesis in magnetotactic bacteria [J]. ACS Chemical Biology, 2017, 12(12): 1-13

[28] ProzorovT, PaloP, WangL-j, Nilsen-HamiltonM, JonesD, OrrD, MallapragadaS K, NarasimhanB, CanfieldP C, ProzorovR. Cobalt ferrite nanocrystals: Out-performing magnetotactic bacteria [J]. ACSNano, 2007, 1(1): 3-228

[29] StanilandS, WilliamsW, TellingN, van der LaanG, HarrisonA, WardB. Controlled cobalt doping of magnetosomes in vivo [J]. Nature Nanotechnology, 2008, 3(3): 158-162

[30] CokerV S, TellingN D, van der LaanG, PattrickRAD, PearceC I, ArenholzE, TunaF, WinpennyR P, LloydJ R. Harnessing the extracellular bacterial production of nanoscale cobalt ferrite with exploitable magnetic properties [J]. ACS Nano, 2009, 3(3): 7-1922

[31] FangJ-h, LiuY, HeW-l, QinW-q, QiuG-z, WangJun. Transformation of iron in pure culture process of extremely acidophilic microorganisms [J]. Transactions of Nonferrous Metals Society of China, 2017, 27(27): 5-1150

[32] YanL, LiP-y, ZhaoX-p, JiR, ZhaoL-juan. Physiological and metabolic responses of maize (Zea mays) plants to Fe₃O₄ nanoparticles [J]. Science of the Total Environment, 2020, 718137400

[33] WuL-b, YangB-j, WangX-x, WuB-q, HeW-l, GanM, QiuG-z, WangJun. Effects of single and mixed energy sources on intracellular nanoparticles synthesized by Acidithiobacillus ferrooxidans [J]. Minerals, 2019, 9(3): 163

[34] XuH, TanL, CuiH, XuM-y, XiaoY, WuH-y, DongH-g, LiuX-x, QiuG-z, XieJ-ping. Characterization of Pd(II) biosorption in aqueous solution by Shewanella oneidensis MR-1 [J]. Journal of Molecular Liquids, 2018, 255333

[35] ZhouH, ZhangR, HuP, ZengW, XieY, WuC, QiuG. Isolation and characterization of Ferroplasma thermophilum sp nov., a novel extremely acidophilic, moderately thermophilic archaeon and its role in bioleaching of chalcopyrite [J]. Journal of Applied Microbiology, 2008, 1051052-591

[36] ZhaoH-b, WangJ, GanX-w, HuM-h, TaoL, QinW-q, QiuG-zhou. Role of pyrite in sulfuric acid leaching of chalcopyrite: An elimination of poly sulfide by controlling redox potential [J]. Hydrometallurgy, 2016, 164159

[37] WangJ, GanX-w, ZhaoH-b, HuM-h, LiK-y, QinW-q, QiuG-zhou. Dissolution and passivation mechanisms of chalcopyrite during bioleaching: DFT calculation, XPS and electrochemistry analysis [J]. Minerals Engineering, 2016, 98264-278

[38] WangJ, TaoL, ZhaoH-b, HuM-h, ZhengX-h, PengH, GanX-w, XiaoW, CaoP, QinW-q, QiuG-z, WangD-zuo. Cooperative effect of chalcopyrite and bornite interactions during bioleaching by mixed moderately thermophilic culture [J]. Minerals Engineering, 2016, 95: 116

[39] FaivreD, SchuelerD. Magnetotactic Bacteria and Magnetosomes [J]. Chemical Reviews, 2008, 108(108): 11-4875

[40] WangJ, HuM-h, ZhaoH-b, GanM b X-w, QinW-q, QiuG-zhou. Well-controlled column bioleaching of a low-grade copper ore by a novel equipment [J]. Journal of Central South University, 2015, 223318-3325

[41] BazylinskiD A, LefevreC T. Magnetotactic bacteria from extreme environments [J]. Life-Basel, 2013295307

[42] ZhaoH-b, GanX-w, WangJ, TaoL, QinW-q, QiuG-zhou. Stepwise bioleaching of Cu-Zn mixed ores with comprehensive utilization of silver-bearing solid waste through a new technique process [J]. Hydrometallurgy, 2017, 171374

[43] FengY-l, WangH-j, LiH-r, ChenX-p, DuZ-w, KangJ-xing. Effect of iron transformation on Acidithiobacillus ferrooxidans bio-leaching of clay vanadium residue [J]. Journal of Central South University, 2019, 26(4): 796-805

[44] HongM-x, WangX-x, WuL-b, FangC-j, HuangX-t, LiaoR, ZhaoH-b, QiuG-z, WangJun. Intermediates transformation of bornite bioleaching by Leptospirillum ferriphilum and Acidithiobacillus caldus [J]. Minerals, 2019, 9(3): 159

[45] KomeiliA. Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria [J]. Fems Microbiology Reviews, 2012, 36361-232

[46] LinW, BazylinskiD A, XiaoT, WuL-f, PanY-xin. Life with compass: Diversity and biogeography of magnetotactic bacteria [J]. Environmental Microbiology, 2014, 16(9SI): 2646-2658

[47] ScheffelA, GruskaM, FaivreD, LinaroudisA, GraumannP L, PlitzkoJ M, SchulerD. An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria (vol 440, pg 110, 2006) [J]. Nature, 2006, 441(7090): 248

[48] WangJ, LiaoR, TaoL, ZhaoH-b, ZhaiR, QinW-q, QiuG-zhou. A comprehensive utilization of silver-bearing solid wastes in chalcopyrite bioleaching [J]. Hydrometallurgy, 2017, 169152

[49] YanL, YueX-x, ZhangS, ChenP, XuZ-l, LiY, LiH-yu. Biocompatibility evaluation of magnetosomes formed by Acidithiobacillus ferrooxidans [J]. Materials Science & Engineering C-Materials for Biological Applications, 2012, 32327-1802

[50] YanL, ZhangS, ChenP, WangW-d, WangY-j, LiH-yu. Magnetic properties of Acidithiobacillus ferrooxidans [J]. Materials Science & Engineering C-Materials for Biological Applications, 2013, 33(33): 7-4026

[51] GanM, LiJ-y, SunS-j, CaoY-y, ZhengZ-h, ZhuJ-y, LiuX-x, WangJ, QiuG-zhou. The enhanced effect of Acidithiobacillus ferrooxidans on pyrite based Cr(VI) reduction [J]. Chemical Engineering Journal, 2018, 34127

[52] Frontiers in Microbiology, 2014, 5(49

[53] FukudaY, OkamuraY, TakeyamaH, MatsunagaT. Dynamic analysis of a genomic island in Magnetospirillum sp strain AMB-1 reveals how magnetosome synthesis developed [J]. Febs Letters, 2006, 580580): 3-801

[54] UllrichS, KubeM, SchubbeS, ReinhardtR, SchulerD. A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises a magnetosome island which undergoes frequent rearrangements during stationary growth [J]. Journal of Bacteriology, 2005, 187(187): 21-7176

[55] JoglerC, WannerG, KolinkoS, NieblerM, AmannR, PetersenN, KubeM, ReinhardtR, SchuelerD. Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching nitrospira phylum [J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(108): 3-1134

[56] WangJ, ZhaoH-b, QinW-q, QiuG-zhou. Bioleaching of complex polymetallic sulfide ores by mixed culture [J]. Journal of Central South University, 2014, 21(21): 7-2633

[57] WangJ, ZhuS, ZhangY-s, ZhaoH-b, HuM-h, YangC-r, QinW-q, QiuG-zhou. Bioleaching of low-grade copper sulfide ores by Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans [J]. Journal of Central South University, 2014, 21728

[58] ZhaoH-b, ZhangY-s, ZhangX, QianL, SunM-l, YanY, ZhangY-s, WangJ, KimH, QiuG-zhou. The dissolution and passivation mechanism of chalcopyrite in bioleaching: An overview [J]. Minerals Engineering, 2019, 136140

[59] WangJ, ZhaoH-b, ZhuangT, QinW-q, ZhuS, QiuG-zhou. Bioleaching of Pb-Zn-Sn chalcopyrite concentrate in tank bioreactor and microbial community succession analysis [J]. Transactions of Nonferrous Metals Society of China, 2013, 23(23): 12-3758

[60] ZhaoH-b, HuangX-t, HuM-h, ZhangC-y, WangJ, QinW-q, QiuG-zhou. Insights into the surface transformation and electrochemical dissolution process of bornite in bioleaching [J]. Minerals, 2018, 8173