Dispersion of sulfur creates a valuable new growth medium formulation that enables earlier sulfur oxidation in relation to iron oxidation in Acidithiobacillus ferrooxidans cultures.
acidophile
dispersed sulfur
iron oxidation
substrate utilization
sulfur oxidation
Journal
Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
28
05
2021
received:
22
02
2021
accepted:
01
06
2021
pubmed:
5
6
2021
medline:
18
1
2022
entrez:
4
6
2021
Statut:
ppublish
Résumé
Acidithiobacillus ferrooxidans is an acidophilic chemolithoautotroph that is commonly reported to exhibit diauxic population growth behavior where ferrous iron is oxidized before elemental sulfur when both are available, despite the higher energy content of sulfur. We have discovered sulfur dispersion formulations that enables sulfur oxidation before ferrous iron oxidation. The oxidation of dispersed sulfur can lower the culture pH within days below the range where aerobic ferrous iron oxidation can occur. Thus, ferric iron reduction can be observed quickly which had previously been reported over extended incubation periods with untreated sulfur. Therefore, we demonstrate that this substrate utilization pattern is strongly dependent on the cell loading in relation to sulfur concentration, sulfur surface hydrophobicity, and the pH of the culture. Our dispersed sulfur formulation, lig-sulfur, can be used to support the rapid antibiotic selection of plasmid-transformed cells, which is not possible in liquid cultures where ferrous iron is the main source of energy for these acidophiles. Furthermore, we find that media containing lig-sulfur supports higher production of green fluorescent protein compared to media containing ferrous iron. The use of dispersed sulfur is a valuable new tool for the development of engineered A. ferrooxidans strains and it provides a new method to control iron and sulfur oxidation behaviors.
Substances chimiques
Culture Media
0
Sulfur
70FD1KFU70
Iron
E1UOL152H7
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3225-3238Subventions
Organisme : NIH HHS
ID : S10RR027050
Pays : United States
Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Amouric, A. , Brochier-Armanet, C. , Johnson, D. B. , Bonnefoy, V. , & Hallberg, K. B. (2011). Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology, 157(1), 111-122. https://doi.org/10.1099/mic.0.044537-0
Aro, T. , & Fatehi, P. (2017). Production and application of lignosulfonates and sulfonated lignin. Chemsuschem, 10(9), 1861-1877. https://doi.org/10.1002/cssc.201700082
Beck, J. V. (1960). A ferrous-ion-oxidizing bacterium. I. Isolation and some general physiological characteristics. Journal of Bacteriology, 79(4), 502-509.
Beebe, J. L. , & Umbreit, W. W. (1971). Extracellular lipid of Thiobacillus thiooxidans . Journal of Bacteriology, 108(1), 612-614. https://doi.org/10.1128/jb.108.1.612-614.1971
Bird, L. J. , Bonnefoy, V. , & Newman, D. K. (2011). Bioenergetic challenges of microbial iron metabolisms. Trends in Microbiology, 19(7), 330-340. https://doi.org/10.1016/j.tim.2011.05.001
Brasseur, G. , Levican, G. , Bonnefoy, V. , Holmes, D. , Jedlicki, E. , & Lemesle-Meunier, D. (2004). Apparent redundancy of electron transfer pathways via bc1 complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans . Biochimica et Biophysica Acta-Bioenergetics, 1656(2), 114-126. https://doi.org/10.1016/j.bbabio.2004.02.008
Bruscella, P. , Appia-Ayme, C. , Levican, G. , Ratouchniak, J. , Jedlicki, E. , Holmes, D. S. , & Bonnefoy, V. (2007). 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. Microbiology, 153(Pt 1), 102-110. https://doi.org/10.1099/mic.0.2006/000067-0
Cao, Z. , Tsai, S. N. , & Zuo, Y. Y. (2019). An optical method for quantitatively determining the surface free energy of micro- and nanoparticles. Analytical Chemistry, 91(20), 12819-12826. https://doi.org/10.1021/acs.analchem.9b02507
Chao, J. , Wang, W. , Xiao, S. , & Liu, X. (2008). Response of Acidithiobacillus ferrooxidans ATCC 23270 gene expression to acid stress. World Journal of Microbiology and Biotechnology, 24(10), 2103-2109. https://doi.org/10.1007/s11274-008-9715-5
Chaudhuri, R. G. , & Paria, S. (2011). Growth kinetics of sulfur nanoparticles in aqueous surfactant solutions. Journal of Colloid and Interface Science, 354(2), 563-569. https://doi.org/10.1016/j.jcis.2010.11.039
Chen, X.-k , Li, X.-y , Ha, Y.-f , Lin, J.-q , Liu, X.-m , Pang, X. , Lin, J. Q. , & Chen, L. X. (2020). Ferric uptake regulator provides a new strategy for acidophile adaptation to acidic ecosystems. Applied and Environmental Microbiology, 86(11), e00268-00220. https://doi.org/10.1128/AEM.00268-20
Chubukov, V. , Gerosa, L. , Kochanowski, K. , & Sauer, U. (2014). Coordination of microbial metabolism. Nature Reviews Microbiology, 12(5), 327-340. https://doi.org/10.1038/nrmicro3238
DiSpirito, A. A. , Dugan, P. R. , & Tuovinen, O. H. (1983). Sorption of Thiobacillus ferrooxidans to particulate material. Biotechnology and Bioengineering, 25(4), 1163-1168. https://doi.org/10.1002/bit.260250422
Eller, J. C. , & Person, J. T. (1969). US Patent No. 3461080A. U. S. P. a. T. Office.
Esparza, M. , Jedlicki, E. , González, C. , Dopson, M. , & Holmes, D. S. (2019). Effect of CO2 concentration on uptake and assimilation of inorganic carbon in the extreme acidophile Acidithiobacillus ferrooxidans . Frontiers in Microbiology, 10(603), 603. https://doi.org/10.3389/fmicb.2019.00603
Espejo, R. T. , Escobar, B. , Jedlicki, E. , Uribe, P. , & Badilla-Ohlbaum, R. (1988). Oxidation of ferrous iron and elemental sulfur by Thiobacillus ferrooxidans . Applied and Environmental Microbiology, 54(7), 1694-1699.
Espejo, R. T. , & Romero, P. (1987). Growth of Thiobacillus ferrooxidans on elemental sulfur. Applied and Environmental Microbiology, 53(8), 1907-1912.
Falagán, C. , & Johnson, D. B. (2016). Acidithiobacillus ferriphilus sp. nov., a facultatively anaerobic iron- and sulfur-metabolizing extreme acidophile. International Journal of Systematic and Evolutionary Microbiology, 66(1), 206-211. https://doi.org/10.1099/ijsem.0.000698
Frederick, L. R. , Jones, G. E. , & Starkey, R. L. (1956). Effects of medium agitation and wetting agents on oxidation of sulphur by Thiobacillus thiooxidans . The Journal of General Microbiology, 15(2), 329-334. https://doi.org/10.1099/00221287-15-2-329
Gehrke, T. , Telegdi, J. , Thierry, D. , & Sand, W. (1998). Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Applied and Environmental Microbiology, 64(7), 2743-2747. https://doi.org/10.1128/AEM.64.7.2743-2747.1998
Ghosh, W. , & Dam, B. (2009). Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiology Review, 33(6), 999-1043. https://doi.org/10.1111/j.1574-6976.2009.00187.x
Gumulya, Y. , Boxall, N. , Khaleque, H. , Santala, V. , Carlson, R. , & Kaksonen, A. (2018). In a quest for engineering acidophiles for biomining applications: Challenges and opportunities. Genes, 9(2), 116.
Hallberg, K. B. , González-Toril, E. , & Johnson, D. B. (2010). Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles, 14(1), 9-19. https://doi.org/10.1007/s00792-009-0282-y
He, H. , Xia, J.-l , Huang, G.-H , Jiang, H.-C. , Tao, X.-X. , Zhao, Y.-D. , & He, W. (2011). Analysis of the elemental sulfur bio-oxidation by Acidithiobacillus ferrooxidans with sulfur K-edge XANES. World Journal of Microbiology and Biotechnology, 27(8), 1927-1931. https://doi.org/10.1007/s11274-010-0629-7
Hedrich, S. , & Johnson, D. B. (2013). Acidithiobacillus ferridurans sp. nov., an acidophilic iron-, sulfur- and hydrogen-metabolizing chemolithotrophic gammaproteobacterium. International Journal of Systematic and Evolutionary Microbiology, 63(Pt_11), 4018-4025. https://doi.org/10.1099/ijs.0.049759-0
Inaba, Y. , Banerjee, I. , Kernan, T. , & Banta, S. (2018). Transposase-mediated chromosomal integration of exogenous genes in Acidithiobacillus ferrooxidans . Applied and Environmental Microbiology, 84(21), e01381-01318. https://doi.org/10.1128/aem.01381-18
Inaba, Y. , Xu, S. , Vardner, J. T. , West, A. C. , & Banta, S. (2019). Microbially influenced corrosion of stainless steel by Acidithiobacillus ferrooxidans supplemented with pyrite: Importance of thiosulfate. Applied and Environmental Microbiology, 85(21), e01381-01319. https://doi.org/10.1128/AEM.01381-19
Johnson, D. B. , Hedrich, S. , & Pakostova, E. (2017). Indirect redox transformations of iron, copper, and chromium catalyzed by extremely acidophilic bacteria. Frontiers in Microbiology, 8(211), 211. https://doi.org/10.3389/fmicb.2017.00211
Kawabe, Y. , Inoue, C. , Suto, K. , & Chida, T. (2003). Inhibitory effect of high concentrations of ferric ions on the activity of Acidithiobacillus ferrooxidans . Journal of Bioscience and Bioengineering, 96(4), 375-379. https://doi.org/10.1016/S1389-1723(03)90140-X
Kelly, D. P. , & Wood, A. P. (2000). Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. International Journal of Systematic and Evolutionary Microbiology, 50(2), 511-516. https://doi.org/10.1099/00207713-50-2-511
Kernan, T. , Majumdar, S. , Li, X. , Guan, J. , West, A. C. , & Banta, S. (2016). Engineering the iron-oxidizing chemolithoautotroph Acidithiobacillus ferrooxidans for biochemical production. Biotechnology and Bioengineering, 113(1), 189-197. https://doi.org/10.1002/bit.25703
Knickerbocker, C. , Nordstrom, D. K. , & Southam, G. (2000). The role of “blebbing” in overcoming the hydrophobic barrier during biooxidation of elemental sulfur by Thiobacillus thiooxidans . Chemical Geology, 169(3), 425-433. https://doi.org/10.1016/S0009-2541(00)00221-7
Konishi, Y. , Takasaka, Y. , & Asai, S. (1994). Kinetics of growth and elemental sulfur oxidation in batch culture of Thiobacillus ferrooxidans . Biotechnology and Bioengineering, 44(6), 667-673. https://doi.org/10.1002/bit.260440602
Kucera, J. , Bouchal, P. , Lochman, J. , Potesil, D. , Janiczek, O. , Zdrahal, Z. , & Mandl, M. (2013). Ferrous iron oxidation by sulfur-oxidizing Acidithiobacillus ferrooxidans and analysis of the process at the levels of transcription and protein synthesis. Antonie Van Leeuwenhoek, 103(4), 905-919. https://doi.org/10.1007/s10482-012-9872-2
Kucera, J. , Lochman, J. , Bouchal, P. , Pakostova, E. , Mikulasek, K. , Hedrich, S. , Janiczek, O. , Mandl, M. , & Johnson, D. B. (2020). A model of aerobic and anaerobic metabolism of hydrogen in the extremophile Acidithiobacillus ferrooxidans . Frontiers in Microbiology, 11(3003), 610836. https://doi.org/10.3389/fmicb.2020.610836
Kucera, J. , Pakostova, E. , Lochman, J. , Janiczek, O. , & Mandl, M. (2016). Are there multiple mechanisms of anaerobic sulfur oxidation with ferric iron in Acidithiobacillus ferrooxidans? Research in Microbiology, 167(5), 357-366. https://doi.org/10.1016/j.resmic.2016.02.004
Kucera, J. , Sedo, O. , Potesil, D. , Janiczek, O. , Zdrahal, Z. , & Mandl, M. (2016). Comparative proteomic analysis of sulfur-oxidizing Acidithiobacillus ferrooxidans CCM 4253 cultures having lost the ability to couple anaerobic elemental sulfur oxidation with ferric iron reduction. Research in Microbiology, 167(7), 587-594. https://doi.org/10.1016/j.resmic.2016.06.009
Li, X. , West, A. C. , & Banta, S. (2016). Enhancing isobutyric acid production from engineered Acidithiobacillus ferrooxidans cells via media optimization. Biotechnology and Bioengineering, 113(4), 790-796. https://doi.org/10.1002/bit.25837
Liu, Z. , Borne, F. , Ratouchniak, J. , & Bonnefoy, V. (2001). Genetic transfer of IncP, IncQ and IncW plasmids to four Thiobacillus ferrooxidans strains by conjugation. Hydrometallurgy, 59(2), 339-345. https://doi.org/10.1016/S0304-386X(00)00176-6
Monod, J. (1949). The growth of bacterial cultures. Annual Review of Microbiology, 3(1), 371-394. https://doi.org/10.1146/annurev.mi.03.100149.002103
Narang, A. , & Pilyugin, S. S. (2007). Bacterial gene regulation in diauxic and non-diauxic growth. Journal of Theoretical Biology, 244(2), 326-348. https://doi.org/10.1016/j.jtbi.2006.08.007
Norris, P. R. , Falagán, C. , Moya-Beltrán, A. , Castro, M. , Quatrini, R. , & Johnson, D. B. (2020). Acidithiobacillus ferrianus sp. nov.: An ancestral extremely acidophilic and facultatively anaerobic chemolithoautotroph. Extremophiles, 24(2), 329-337. https://doi.org/10.1007/s00792-020-01157-1
Ohmura, N. , Sasaki, K. , Matsumoto, N. , & Saiki, H. (2002). Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans . Journal of Bacteriology, 184(8), 2081-2087. https://doi.org/10.1128/JB.184.8.2081-2087.2002
Okano, H. , Hermsen, R. , Kochanowski, K. , & Hwa, T. (2020). Regulation underlying hierarchical and simultaneous utilization of carbon substrates by flux sensors in Escherichia coli . Nature Microbiology, 5(1), 206-215. https://doi.org/10.1038/s41564-019-0610-7
Osorio, H. , Mangold, S. , Denis, Y. , Ñancucheo, I. , Esparza, M. , Johnson, D. B. , Bonnefoy, V. , Dopson, M. , & Holmes, D. S. (2013). Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans . Applied and Environmental Microbiology, 79(7), 2172-2181. https://doi.org/10.1128/AEM.03057-12
Peng, A.-A. , Liu, H.-c , Nie, Z.-y , & Xia, J.-l (2012). Effect of surfactant Tween-80 on sulfur oxidation and expression of sulfur metabolism relevant genes of Acidithiobacillus ferrooxidans . Transactions of Nonferrous Metals Society of China, 22(12), 3147-3155. https://doi.org/10.1016/S1003-6326(12)61767-1
Peng, J.-B. , Yan, W.-M. , & Bao, X.-Z. (1994). Solid medium for the genetic manipulation of Thiobacillus ferrooxidans . The Journal of General and Applied Microbiology, 40(3), 243-253. https://doi.org/10.2323/jgam.40.243
Ponce, J. S. , Moinier, D. , Byrne, D. , Amouric, A. , & Bonnefoy, V. (2012). Acidithiobacillus ferrooxidans oxidizes ferrous iron before sulfur likely through transcriptional regulation by the global redox responding RegBA signal transducing system. Hydrometallurgy, 127-128, 187-194. https://doi.org/10.1016/j.hydromet.2012.07.016
Pronk, J. T. , de Bruyn, J. C. , Bos, P. , & Kuenen, J. G. (1992). Anaerobic growth of Thiobacillus ferrooxidans . Applied and Environmental Microbiology, 58(7), 2227-2230.
Qiu, X. , Kong, Q. , Zhou, M. , & Yang, D. (2010). Aggregation behavior of sodium lignosulfonate in water solution. The Journal of Physical Chemistry B, 114(48), 15857-15861. https://doi.org/10.1021/jp107036m
Quatrini, R. , Appia-Ayme, C. , Denis, Y. , Jedlicki, E. , Holmes, D. S. , & Bonnefoy, V. (2009). Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans . BMC Genomics, 10, 394. https://doi.org/10.1186/1471-2164-10-394
Ramirez, P. , Guiliani, N. , Valenzuela, L. , Beard, S. , & Jerez, C. A. (2004). Differential protein expression during growth of Acidithiobacillus ferrooxidans on ferrous iron, sulfur compounds, or metal sulfides. Applied and Environmental Microbiology, 70(8), 4491-4498. https://doi.org/10.1128/aem.70.8.4491-4498.2004
Sand, W. (1989). Ferric iron reduction by Thiobacillus ferrooxidans at extremely low pH-values. Biogeochemistry, 7(3), 195-201. https://doi.org/10.1007/BF00004217
Schaeffer, W. I. , & Umbreit, W. W. (1963). Phosphotidylinositol as a wetting agent in sulfur oxidation by Thiobacillus thiooxidans . Journal of Bacteriology, 85(2), 492-493.
Smith, S. L. , & Johnson, D. B. (2018). Growth of Leptospirillum ferriphilum in sulfur medium in co-culture with Acidithiobacillus caldus . Extremophiles, 22(2), 327-333. https://doi.org/10.1007/s00792-018-1001-3
Suzuki, I. , Takeuchi, T. L. , Yuthasastrakosol, T. D. , & Oh, J. K. (1990). Ferrous iron and sulfur oxidation and ferric iron reduction activities of Thiobacillus ferrooxidans are affected by growth on ferrous iron, sulfur, or a sulfide ore. Applied and Environmental Microbiology, 56(6), 1620-1626.
Terpilowski, K. , Holysz, L. , & Chibowski, E. (2008). Surface free energy of sulfur-Revisited: II. Samples solidified against different solid surfaces. Journal of Colloid and Interface Science, 319(2), 514-519. https://doi.org/10.1016/j.jcis.2007.10.054
Valdés, J. , Pedroso, I. , Quatrini, R. , Dodson, R. J. , Tettelin, H. , Blake, R., 2nd , Eisen, J. A. , & Holmes, D. S. (2008). Acidithiobacillus ferrooxidans metabolism: From genome sequence to industrial applications. BMC Genomics, 9, 597. https://doi.org/10.1186/1471-2164-9-597
Wang, H. , Liu, X. , Liu, S. , Yu, Y. , Lin, J. , Lin, J. , Pang, X. , & Zhao, J. (2012). Development of a markerless gene replacement system for Acidithiobacillus ferrooxidans and construction of a pfkB mutant. Applied and Environmental Microbiology, 78(6), 1826-1835. https://doi.org/10.1128/AEM.07230-11
Wang, R. , Lin, C. , Lin, J. , Pang, X. , Liu, X. , Zhang, C. , Lin, J. , & Chen, L. (2017). Construction of novel pJRD215-derived plasmids using chloramphenicol acetyltransferase (cat) gene as a selection marker for Acidithiobacillus caldus . PLOS One, 12(8), e0183307. https://doi.org/10.1371/journal.pone.0183307
Wong, P. , Gladney, S. , & Keasling, J. D. (1997). Mathematical model of the lac operon: Inducer exclusion, catabolite repression, and diauxic growth on glucose and lactose. Biotechnology Progress, 13(2), 132-143. https://doi.org/10.1021/bp970003o
Wu, L. , Yang, B. , Wang, X. , Wu, B. , He, W. , Gan, M. , Qiu, G. , & Wang, J. (2019). Effects of single and mixed energy sources on intracellular nanoparticles synthesized by Acidithiobacillus ferrooxidans . Minerals, 9(3), 163.
Xia, L.-X. , Shen, Z. , Vargas, T. , Sun, W.-J. , Ruan, R.-M. , Xie, Z.-D. , & Qiu, G.-Z. (2013). Attachment of Acidithiobacillus ferrooxidans onto different solid substrates and fitting through Langmuir and Freundlich equations. Biotechnology Letters, 35(12), 2129-2136. https://doi.org/10.1007/s10529-013-1316-1
Yarzabal, A. , Appia-Ayme, C. , Ratouchniak, J. , & Bonnefoy, V. (2004). Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology, 150(Pt 7), 2113-2123. https://doi.org/10.1099/mic.0.26966-0
Yu, Y. , Liu, X. , Wang, H. , Li, X. , & Lin, J. (2014). Construction and characterization of tetH overexpression and knockout strains of Acidithiobacillus ferrooxidans . Journal of Bacteriology, 196(12), 2255-2264. https://doi.org/10.1128/JB.01472-13
Zhang, Y. , Yang, Y. , Liu, J. , & Qiu, G. (2013). Isolation and characterization of Acidithiobacillus ferrooxidans strain QXS-1 capable of unusual ferrous iron and sulfur utilization. Hydrometallurgy, 136, 51-57. https://doi.org/10.1016/j.hydromet.2013.03.005