Application of Acidithiobacillus spp. in Industry and Agriculture

doi:10.13560/j.cnki.biotech.bull.1985.2022-0139

Abstract

Abstract:

Acidithiobacillus spp. are acidophilic chemolithotrophic gram-negative bacteria and capable of oxidizing ferrous iron,sulfur or reduced inorganic sulfur compounds（RISCs）to obtain energy and fix carbon dioxide. Acidithiobacillus spp. are widely distributed in acidic mineral water,hot spring and other acidic environments,and are the main promoter of sulfur and iron cycling in the Earth’s ecosystems. Members of this genus are widely used in the field of bioleaching for the unique metabolic characteristics and extreme environmental adaptability. In this paper,the physiological and metabolic characteristics of Acidithiobacillus spp.and the adaptation mechanism in extreme environments are reviewed,and the application of Acidithiobacillus spp. in industry and agriculture is expounded. The main research directions and key scientific issues to be solved in the future for major national needs are discussed,which provided important clues and enlightenment for the research of Acidithiobacillus spp. in physiological metabolism,environmental adaptation and industrial and agricultural applications.

Key words: Acidithiobacillus, extreme environment, sulfur metabolism, iron metabolism, bioleaching

GAO Xue-yan, CHEN Lin-xu, CHEN Xian-ke, PANG Xin, PAN Deng, LIN Jian-qun. Application of Acidithiobacillus spp. in Industry and Agriculture[J]. Biotechnology Bulletin, 2022, 38(5): 36-46.

Figures/Tables 3

References 67

[1]	Sriaporn C, Campbell KA, van Kranendonk MJ, et al. Genomic adaptations enabling Acidithiobacillus distribution across wide-ranging hot spring temperatures and pHs[J]. Microbiome, 2021, 9(1):135. doi: 10.1186/s40168-021-01090-1 URL
[2]	Liu YJ, Wu SL, Southam G, et al. Bioaugmentation with Acidithiobacillus species accelerates mineral weathering and formation of secondary mineral cements for hardpan development in sulfidic Pb-Zn tailings[J]. J Hazard Mater, 2021, 411:124988. doi: 10.1016/j.jhazmat.2020.124988 URL
[3]	Vishniac W, Santer M. The thiobacilli[J]. Bacteriol Rev, 1957, 21(3):195-213. doi: 10.1128/br.21.3.195-213.1957 URL
[4]	Wang R, Lin JQ, Liu XM, et al. Sulfur oxidation in the acidophilic autotrophic Acidithiobacillus spp[J]. Front Microbiol, 2019, 9:3290. doi: 10.3389/fmicb.2018.03290 URL
[5]	Schrenk MO, Edwards KJ, Goodman RM, et al. Distribution of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans:implications for generation of acid mine drainage[J]. Science, 1998, 279(5356):1519-1522. pmid: 9488647
[6]	Hallberg KB, González-Toril E, Johnson DB. Acidithiobacillus ferrivorans, sp. nov.;facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments[J]. Extremophiles, 2010, 14(1):9-19. doi: 10.1007/s00792-009-0282-y pmid: 19787416
[7]	Hedrich S, Johnson DB. Acidithiobacillus ferridurans sp. nov., an acidophilic iron-, sulfur- and hydrogen-metabolizing chemolithotrophic gammaproteobacterium[J]. Int J Syst Evol Microbiol, 2013, 63(Pt_11):4018-4025. doi: 10.1099/ijs.0.049759-0 URL
[8]	Falagán C, Johnson DB. Acidithiobacillus ferriphilus sp. nov., a facultatively anaerobic iron- and sulfur-metabolizing extreme acidophile[J]. Int J Syst Evol Microbiol, 2016, 66(1):206-211. doi: 10.1099/ijsem.0.000698 URL
[9]	Norris PR, Falagán C, Moya-Beltrán A, et al. Acidithiobacillus ferrianus sp. nov. :an ancestral extremely acidophilic and facultatively anaerobic chemolithoautotroph[J]. Extremophiles, 2020, 24(2):329-337. doi: 10.1007/s00792-020-01157-1 pmid: 31980944
[10]	Yang L, Zhao D, Yang J, et al. Acidithiobacillus thiooxidans and its potential application[J]. Appl Microbiol Biotechnol, 2019, 103(19):7819-7833. doi: 10.1007/s00253-019-10098-5 pmid: 31463545
[11]	Chen LX, Ren YL, Lin JQ, et al. Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant[J]. PLoS One, 2012, 7(9):e39470. doi: 10.1371/journal.pone.0039470 URL
[12]	Castro M, Moya-Beltrán A, Covarrubias PC, et al. Draft genome sequence of the type strain of the sulfur-oxidizing acidophile, Acidithiobacillus albertensis(DSM 14366)[J]. Stand Genomic Sci, 2017, 12:77. doi: 10.1186/s40793-017-0282-y URL
[13]	Falagán C, Moya-Beltrán A, Castro M, et al. Acidithiobacillus sulfuriphilus sp. nov. :an extremely acidophilic sulfur-oxidizing chemolithotroph isolated from a neutral pH environment[J]. Int J Syst Evol Microbiol, 2019, 69(9):2907-2913. doi: 10.1099/ijsem.0.003576 URL
[14]	Hedrich S, Johnson DB. Aerobic and anaerobic oxidation of hydrogen by acidophilic bacteria[J]. FEMS Microbiol Lett, 2013, 349(1):40-45.
[15]	Bosecker K. Bioleaching:metal solubilization by microorganisms[J]. FEMS Microbiol Rev, 1997, 20(3/4):591-604. doi: 10.1111/j.1574-6976.1997.tb00340.x URL
[16]	Rohwerder T, Gehrke T, Kinzler K, et al. Bioleaching review part A:progress in bioleaching:fundamentals and mechanisms of bacterial metal sulfide oxidation[J]. Appl Microbiol Biotechnol, 2003, 63(3):239-248. pmid: 14566432
[17]	Mangold S, Valdés J, Holmes DS, et al. Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus[J]. Front Microbiol, 2011, 2:17.
[18]	Quatrini R, Appia-Ayme C, Denis Y, et al. Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans[J]. BMC Genomics, 2009, 10:394. doi: 10.1186/1471-2164-10-394 pmid: 19703284
[19]	Valdés J, Pedroso I, Quatrini R, et al. Acidithiobacillus ferrooxidans metabolism:from genome sequence to industrial applications[J]. BMC Genom, 2008, 9:597. doi: 10.1186/1471-2164-9-597 URL
[20]	Feng SS, Yang HL, Wang W. System-level understanding of the potential acid-tolerance components of Acidithiobacillus thiooxidans ZJJN-3 under extreme acid stress[J]. Extremophiles, 2015, 19(5):1029-1039. doi: 10.1007/s00792-015-0780-z URL
[21]	Li LF, Fu LJ, Lin JQ, et al. The σ 54-dependent two-component system regulating sulfur oxidization(Sox)system in Acidithio-bacillus caldus and some chemolithotrophic bacteria[J]. Appl Microbiol Biotechnol, 2017, 101(5):2079-2092. doi: 10.1007/s00253-016-8026-2 pmid: 27966049
[22]	Ingledew WJ. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph[J]. Biochim Biophys Acta, 1982, 683(2):89-117. pmid: 6295474
[23]	Bruscella P, Appia-Ayme C, Levicán G, et al. Differential expression of two bc1 complexes in the strict acidophilic chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans suggests a model for their respective roles in iron or sulfur oxidation[J]. Microbiology(Reading), 2007, 153(Pt 1):102-110.
[24]	Yarzábal A, Appia-Ayme C, Ratouchniak J, et al. Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin[J]. Microbiology(Reading), 2004, 150(Pt 7):2113-2123.
[25]	Yarzábal A, Duquesne K, Bonnefoy V. Rusticyanin gene expression of Acidithiobacillus ferrooxidans ATCC 33020 in sulfur- and in ferrous iron media[J]. Hydrometallurgy, 2003, 71(1/2):107-114. doi: 10.1016/S0304-386X(03)00146-4 URL
[26]	Kucera J, Lochman J, Bouchal P, et al. A model of aerobic and anaerobic metabolism of hydrogen in the extremophile Acidithiobacillus ferrooxidans[J]. Front Microbiol, 2020, 11:610836. doi: 10.3389/fmicb.2020.610836 URL
[27]	Lacasse MJ, Zamble DB. NiFe]-hydrogenase maturation[J]. Biochemistry, 2016, 55(12):1689-1701. doi: 10.1021/acs.biochem.5b01328 URL
[28]	Adams MWW, Mortenson LE, Chen JS. Hydrogenase[J]. Biochim Biophys Acta BBA Rev Bioenerg, 1980, 594(2/3):105-176.
[29]	Fischer J, Quentmeier A, Kostka S, et al. Purification and characterization of the hydrogenase from Thiobacillus ferrooxidans[J]. Arch Microbiol, 1996, 165(5):289-296. pmid: 8661919
[30]	Schröder O, Bleijlevens B, de Jongh TE, et al. Characterization of a cyanobacterial-like uptake[NiFe]hydrogenase:EPR and FTIR spectroscopic studies of the enzyme from Acidithiobacillus ferrooxidans[J]. J Biol Inorg Chem, 2007, 12(2):212-233. pmid: 17082918
[31]	Gao XY, Fu CG, Hao LK, et al. The substrate-dependent regulatory effects of the AfeI/R system in Acidithiobacillus ferrooxidans reveals the novel regulation strategy of quorum sensing in acidophiles[J]. Environ Microbiol, 2021, 23(2):757-773. doi: 10.1111/1462-2920.15163 URL
[32]	Whiteley M, Diggle SP, Greenberg EP. Progress in and promise of bacterial quorum sensing research[J]. Nature, 2017, 551(7680):313-320. doi: 10.1038/nature24624 URL
[33]	Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria[J]. Nat Rev Microbiol, 2016, 14(9):576-588. doi: 10.1038/nrmicro.2016.89 pmid: 27510864
[34]	Farah C, Vera M, Morin D, et al. Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans[J]. Appl Environ Microbiol, 2005, 71(11):7033-7040. doi: 10.1128/AEM.71.11.7033-7040.2005 URL
[35]	Rivas M, Seeger M, Holmes DS, et al. A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus ferrooxidans[J]. Biol Res, 2005, 38(2/3):283-297.
[36]	Qiu CS, Xie SY, Liu NN, et al. Removal behavior and chemical speciation distributions of heavy metals in sewage sludge during bioleaching and combined bioleaching/Fenton-like processes[J]. Sci Rep, 2021, 11(1):14879. doi: 10.1038/s41598-021-94216-2 URL
[37]	Rivas M, Seeger M, Jedlicki E, et al. Second acyl homoserine lactone production system in the extreme acidophile Acidithiobacillus ferrooxidans[J]. Appl Environ Microbiol, 2007, 73(10):3225-3231. doi: 10.1128/AEM.02948-06 URL
[38]	González A, Bellenberg S, Mamani S, et al. AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans[J]. Appl Microbiol Biotechnol, 2013, 97(8):3729-3737. doi: 10.1007/s00253-012-4229-3 pmid: 22752316
[39]	Bellenberg S, Díaz M, Noël N, et al. Biofilm formation, communication and interactions of leaching bacteria during colonization of pyrite and sulfur surfaces[J]. Res Microbiol, 2014, 165(9):773-781. doi: 10.1016/j.resmic.2014.08.006 pmid: 25172572
[40]	Mamani S, Moinier D, Denis Y, et al. Insights into the quorum sensing regulon of the acidophilic Acidithiobacillus ferrooxidans revealed by transcriptomic in the presence of an acyl homoserine lactone superagonist analog[J]. Front Microbiol, 2016, 7:1365. doi: 10.3389/fmicb.2016.01365 pmid: 27683573
[41]	Narla AV, Borenstein DB, Wingreen NS. A biophysical limit for quorum sensing in biofilms[J]. PNAS, 2021, 118(21):e2022818118.
[42]	Gao XY, Liu XJ, Fu CA, et al. Novel strategy for improvement of the bioleaching efficiency of Acidithiobacillus ferrooxidans based on the AfeI/R quorum sensing system[J]. Minerals, 2020, 10(3):222. doi: 10.3390/min10030222 URL
[43]	Teitzel GM, Parsek MR. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa[J]. Appl Environ Microbiol, 2003, 69(4):2313-2320. doi: 10.1128/AEM.69.4.2313-2320.2003 URL
[44]	Nies DH. Efflux-mediated heavy metal resistance in prokaryotes[J]. FEMS Microbiol Rev, 2003, 27(2/3):313-339.
[45]	Alvarez S, Jerez CA. Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans[J]. Appl Environ Microbiol, 2004, 70(9):5177-5182. doi: 10.1128/AEM.70.9.5177-5182.2004 URL
[46]	Navarro CA, von Bernath D, Jerez CA. Heavy metal resistance strategies of acidophilic bacteria and their acquisition:importance for biomining and bioremediation[J]. Biol Res, 2013, 46(4):363-371. doi: 10.4067/S0716-97602013000400008 URL
[47]	Baker-Austin C, Dopson M. Life in acid:pH homeostasis in acidophiles[J]. Trends Microbiol, 2007, 15(4):165-171. pmid: 17331729
[48]	Krulwich TA, Sachs G, Padan E. Molecular aspects of bacterial pH sensing and homeostasis[J]. Nat Rev Microbiol, 2011, 9(5):330-343. doi: 10.1038/nrmicro2549 pmid: 21464825
[49]	Mykytczuk NCS, Trevors JT, Ferroni GD, et al. Cytoplasmic membrane fluidity and fatty acid composition of Acidithiobacillus ferrooxidans in response to pH stress[J]. Extremophiles, 2010, 14(5):427-441. doi: 10.1007/s00792-010-0319-2 pmid: 20582711
[50]	Tyson GW, Chapman J, Hugenholtz P, et al. Community structure and metabolism through reconstruction of microbial genomes from the environment[J]. Nature, 2004, 428(6978):37-43. doi: 10.1038/nature02340 URL
[51]	Nguyen TH, Won S, Ha MG, et al. Bioleaching for environmental remediation of toxic metals and metalloids:a review on soils, sediments, and mine tailings[J]. Chemosphere, 2021, 282:131108. doi: 10.1016/j.chemosphere.2021.131108 URL
[52]	Mousavi SM, Yaghmaei S, Vossoughi M, et al. Zinc extraction from Iranian low-grade complex zinc-lead ore by two native microorganisms:Acidithiobacillus ferrooxidans and Sulfobacillus[J]. Int J Miner Process, 2006, 80(2/3/4):238-243. doi: 10.1016/j.minpro.2006.05.001 URL
[53]	Yang CR, Qin WQ, Lai SS, et al. Bioleaching of a low grade nickel-copper-cobalt sulfide ore[J]. Hydrometallurgy, 2011, 106(1/2):32-37. doi: 10.1016/j.hydromet.2010.11.013 URL
[54]	Romo E, Weinacker DF, Zepeda AB, et al. Bacterial consortium for copper extraction from sulphide ore consisting mainly of chalcopyrite[J]. Braz J Microbiol, 2013, 44(2):523-528. doi: 10.1590/S1517-83822013005000043 pmid: 24294251
[55]	Roy JJ, Cao B, Madhavi S. A review on the recycling of spent lithium-ion batteries(LIBs)by the bioleaching approach[J]. Chemosphere, 2021, 282:130944. doi: 10.1016/j.chemosphere.2021.130944 URL
[56]	Forti V.; Baldé C. P.; Kuehr R., et al. The Global E-waste Monitor 2020. Quantities, flows, and the circular economy potential[M]. Bonn/Geneva/Rotterdam:United Nations University(UNU)/United Nations Institute for Training and Research(UNITAR)- co-hosted SCYCLE Programme, International Telecommunication Union(ITU)& International Solid Waste Association(ISWA), 2020.
[57]	Kadivar S, Pourhossein F, Mousavi SM. Recovery of valuable metals from spent mobile phone printed circuit boards using biochar in indirect bioleaching[J]. J Environ Manag, 2021, 280:111642. doi: 10.1016/j.jenvman.2020.111642 URL
[58]	Pourhossein F, Mousavi SM. A novel step-wise indirect bioleaching using biogenic ferric agent for enhancement recovery of valuable metals from waste light emitting diode(WLED)[J]. J Hazard Mater, 2019, 378:120648. doi: 10.1016/j.jhazmat.2019.05.041 URL
[59]	第二次全国污染源普查公报[J]. 环境保护, 2020, 48(18):8-10.
	The second national pollution source census bulletin[J]. Environ Prot, 2020, 48(18):8-10.
[60]	Kremser K, Thallner S, Strbik D, et al. Leachability of metals from waste incineration residues by iron- and sulfur-oxidizing bacteria[J]. J Environ Manage, 2021, 280:111734. doi: 10.1016/j.jenvman.2020.111734 URL
[61]	Gholami RM, Borghei SM, Mousavi SM. Bacterial leaching of a spent Mo-Co-Ni refinery catalyst using Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans[J]. Hydrometallurgy, 2011, 106(1/2):26-31. doi: 10.1016/j.hydromet.2010.11.011 URL
[62]	Cheng R, Zhou W, Lin L, et al. Removal of high concentrations of H₂S from simulated natural gas by Acidithiobacillus ferrooxidans immobilized on polyurethane foam[J]. J Chem Technol Biotechnol, 2013, 88(5):975-978.
[63]	Liu FW, Lei YS, Shi J, et al. Effect of microbial nutrients supply on coal bio-desulfurization[J]. J Hazard Mater, 2020, 384:121324. doi: 10.1016/j.jhazmat.2019.121324 URL
[64]	McFarland BL. Biodesulf urization[J]. Curr Opin Microbiol, 1999, 2(3):257-264. pmid: 10383871
[65]	Kiragosyan K, Picard M, Timmers PHA, et al. Effect of methanethiol on process performance, selectivity and diversity of sulfur-oxidizing bacteria in a dual bioreactor gas biodesulfurization system[J]. J Hazard Mater, 2020, 398:123002. doi: 10.1016/j.jhazmat.2020.123002 URL
[66]	Waksman SA, Joffe JS. Acid production by a new sulfur-oxidizing bacterium[J]. Science, 1921, 53(1366):216. pmid: 17831199
[67]	Nareshkumar R, Nagendran R, Parvathi K. Bioleaching of heavy metals from contaminated soil using Acidithiobacillus thiooxidans:effect of sulfur/soil ratio[J]. World J Microbiol Biotechnol, 2008, 24(8):1539-1546. doi: 10.1007/s11274-007-9639-5 URL

菌种 Species	生长pH值 Growth pH	硫代谢能力 Sulfur metab- olism ability	铁代谢能力 Iron metabo- lism ability	氢代谢能力 Hydrogen met- abolism ability
A. ferrooxidans^[4]	1.3-4.5	+	+	+
A. ferrivorans^{[6⇓⇓⇓⇓⇓⇓⇓,14]}	1.9-3.4	+	+	（+）
A. ferriphilus^[8]	1.5-	+	+	-
A. ferridurans^[7]	1.4-3.0	+	+	+
A. ferrianus^[9]	1.3-3.7	+	+	+
A. thiooxidans^[4]	0.5-5.5	+	-	-
A. caldus^[4]	1.0-3.5	+	-	+
A. albertensis^{[4⇓⇓⇓⇓⇓⇓⇓,12]}	0.5-6.0	+	-	NR
A. sulfuriphilus^[13]	1.8-7.0	+	-	-

菌种 Species	生长pH值 Growth pH	硫代谢能力 Sulfur metab- olism ability	铁代谢能力 Iron metabo- lism ability	氢代谢能力 Hydrogen met- abolism ability
A. ferrooxidans^[4]	1.3-4.5	+	+	+
A. ferrivorans^{[6⇓⇓⇓⇓⇓⇓⇓,14]}	1.9-3.4	+	+	（+）
A. ferriphilus^[8]	1.5-	+	+	-
A. ferridurans^[7]	1.4-3.0	+	+	+
A. ferrianus^[9]	1.3-3.7	+	+	+
A. thiooxidans^[4]	0.5-5.5	+	-	-
A. caldus^[4]	1.0-3.5	+	-	+
A. albertensis^{[4⇓⇓⇓⇓⇓⇓⇓,12]}	0.5-6.0	+	-	NR
A. sulfuriphilus^[13]	1.8-7.0	+	-	-