Skip to main content
SpringerLink
Log in

Active fluid with Acidithiobacillus ferrooxidans: correlations between swimming and the oxidation route

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

To explore engineering platforms towards ‘active bacterial baths’, we grow and characterize native and commercial strains of Acidithiobacillus ferrooxidans to promote swimming locomotion. Three different energy sources were used, namely elemental sulfur, ferrous sulfate, and pyrite. The characteristics of the culture, such as pH, Eh, and the concentration of cells and ions, are monitored to seek correlations between the oxidation route and the transport mechanism. We found that only elemental sulfur induces swimming mobility in the commercial DSMZ – 24,419 strain, while ferrous sulfate and the sulfide mineral, pyrite, did not activate swimming on any strain. The bacterial mean squared displacement and the mean velocity are measured to provide a quantitative description of the bacterial mobility. We found that, even if the A. ferrooxidans strain is grown in a sulfur-rich environment, it preferentially oxidizes iron when an iron-based material is included in the media. Similar to other species, once the culture pH decreases below 1.2, the active locomotion is inhibited. The engineering control and activation of swimming in bacterial cultures offer fertile grounds towards applications of active suspensions such as energy-efficient bioleaching, mixing, drug delivery, and bio-sensing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  1. Goodrich, C.P., Brenner, M.P.: Using active colloids as machines to weave and braid on the micrometer scale. Proc. Natl. Acad. Sci. U.S.A. 114, 257–262 (2017). https://doi.org/10.1073/pnas.1608838114

  2. Keber, F., Loiseau, E., Sanchez, T., DeCamp, S., Giomi, L., Bowick, M., Marchetti, M.C., Dogic, Z., Bausch, A.: Topology and dynamics of active nematic vesicles. Science 345, 1135–1139 (2014). https://doi.org/10.1126/science.1254784

  3. Thampi, S.P., Doostmohammadi, A., Shendruk, T.N., Golestanian, R., Yeomans, J.M.: Active micromachines: microfluidics powered by mesoscale turbulence. Sci. Adv. 2, e1501854 (2016). https://doi.org/10.1126/sciadv.1501854

    Article  ADS  Google Scholar 

  4. Takatori, S.C., Brady, J.F.: Towards a thermodynamics of active matter. Phys. Rev. E. 91, (2015). https://doi.org/10.1103/PhysRevE.91.032117

  5. Takatori, S.C., Brady, J.F.: Swim stress, motion, and deformation of active matter: effect of an external field. Soft Matter 10, 9433–9445 (2014). https://doi.org/10.1039/C4SM01409J

    Article  ADS  Google Scholar 

  6. Takatori, S.C., Yan, W., Brady, J.F.: Swim pressure: stress generation in active matter. Phys. Rev. Lett. 113, 1–5 (2014). https://doi.org/10.1103/PhysRevLett.113.028103

    Article  Google Scholar 

  7. Saintillan, D., Shelley, M.J.: Instabilities, pattern formation, and mixing in active suspensions. Phys. Fluids 20, 123304 (2008). https://doi.org/10.1063/1.3041776

    Article  ADS  MATH  Google Scholar 

  8. Ezhilan, B., Pahlavan, A.A., Saintillan, D.: Chaotic dynamics and oxygen transport in thin films of aerotactic bacteria. Phys. Fluids 24, (2012). https://doi.org/10.1063/1.4752764

  9. Saintillan, D., Shelley, M.J.: Emergence of coherent structures and large-scale flows in motile suspensions. J. R. Soc. Interface 9, 571–585 (2012). https://doi.org/10.1098/rsif.2011.0355

    Article  Google Scholar 

  10. Wensink, H.H., Dunkel, J., Heidenreich, S., Drescher, K., Goldstein, R.E., Lowen, H., Yeomans, J.M.: Meso-scale turbulence in living fluids. Proc. Natl. Acad. Sci. U.S.A. 109, 14308–14313 (2012). https://doi.org/10.1073/pnas.1202032109

  11. Alexander, G.P., Yeomans, J.M.: Dumb-bell swimmers. Europhys. Lett. 83, (2008). https://doi.org/10.1209/0295-5075/83/34006

  12. Dunkel, J., Putz, V.B., Zaid, I.M., Yeomans, J.M.: Swimmer–tracer scattering at low Reynolds number. Soft Matter 6, 4268–4276 (2010). https://doi.org/10.1039/c0sm00164c

  13. Hernandez-Ortiz, J.P., Stoltz, C.G., Graham, M.D.: Transport and collective dynamics in suspensions of confined swimming particles. Phys. Rev. Lett. 95, 1–4 (2005). https://doi.org/10.1103/PhysRevLett.95.204501

    Article  Google Scholar 

  14. Underhill, P.T., Hernandez-Ortiz, J.P., Graham, M.D.: Diffusion and spatial correlations in suspensions of swimming particles. Phys. Rev. Lett. 100, 1–4 (2008). https://doi.org/10.1103/PhysRevLett.100.248101

    Article  Google Scholar 

  15. Hernandez-Ortiz, J.P., Underhill, P.T., Graham, M.D.: Dynamics of confined suspensions of swimming particles. J. Phys. Condens. Matter. 21, (2009). https://doi.org/10.1088/0953-8984/21/20/204107

  16. Kolmakov, G.V., Schaefer, A., Aranson, I., Balazs, A.C.: Designing mechano-responsive microcapsules that undergo self-propelled motion. Soft Matter 8, 180–190 (2012). https://doi.org/10.1039/C1SM06415K

    Article  ADS  Google Scholar 

  17. Guasto, J.S., Rusconi, R., Stocker, R.: Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44, 373–400 (2012). https://doi.org/10.1146/annurev-fluid-120710-101156

    Article  ADS  MathSciNet  MATH  Google Scholar 

  18. Sokolov, A., Aranson, I.S.: Physical properties of collective motion in suspensions of bacteria. Phys. Rev. Lett. 109, 1–5 (2012). https://doi.org/10.1103/PhysRevLett.109.248109

    Article  Google Scholar 

  19. Zhou, S., Sokolov, A., Lavrentovich, O.D., Aranson, I.S.: Living liquid crystals. Proc. Natl. Acad. Sci. U.S.A. 111, 1265–1270 (2014). https://doi.org/10.1073/pnas.1321926111

  20. Miño, G.L., Dunstan, J., Rousselet, A., Clément, E., Soto, R.: Induced diffusion of tracers in a bacterial suspension: theory and experiments. J. Fluid Mech. 729, 423–444 (2013). https://doi.org/10.1017/jfm.2013.304

    Article  ADS  MATH  Google Scholar 

  21. Calle-Castañeda, S.M., Márquez-Godoy, M.A., Hernández-Ortiz, J.P.: Solubilization of phosphorus from phosphate rocks with Acidithiobacillus thiooxidans following a growing-then-recovery process. World J. Microbiol. Biotechnol. 34, (2018). https://doi.org/10.1007/s11274-017-2390-7

  22. Calle-Castañeda, S.M., Márquez-Godoy, M.A., Hernández-Ortiz, J.P.: Phosphorus recovery from high concentrations of low-grade phosphate rocks using the biogenic acid produced by the acidophilic bacteria Acidithiobacillus thiooxidans. Miner. Eng. 115, 97–105 (2018). https://doi.org/10.1016/j.mineng.2017.10.014

    Article  Google Scholar 

  23. Drescher, K., Dunkel, J., Cisneros, L.H., Ganguly, S., Goldstein, R.E.: Fluid dynamics and noise in bacterial cell–cell and cell–surface scattering. Proc. Natl. Acad. Sci. 108, 10940–10945 (2011). https://doi.org/10.1073/pnas.1019079108/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1019079108

    Article  ADS  Google Scholar 

  24. Gyrya, V., Aranson, I.S., Berlyand, L.V., Karpeev, D.: A model of hydrodynamic interaction between swimming bacteria. Bull. Math. Biol. 72, 148–183 (2010). https://doi.org/10.1007/s11538-009-9442-6

    Article  MathSciNet  MATH  Google Scholar 

  25. Berke, A.P., Turner, L., Berg, H.C., Lauga, E.: Hydrodynamic attraction of swimming microorganisms by surfaces. Phys. Rev. Lett. 101, 1–5 (2008). https://doi.org/10.1103/PhysRevLett.101.038102

    Article  Google Scholar 

  26. Micali, G., Endres, R.G.: Bacterial chemotaxis: information processing, thermodynamics, and behavior. Curr. Opin. Microbiol. 30, 8–15 (2016). https://doi.org/10.1016/j.mib.2015.12.001

    Article  Google Scholar 

  27. Carlsen, R.W., Sitti, M.: Bio-hybrid cell-based actuators for microsystems. Small 10, 3831–3851 (2014). https://doi.org/10.1002/smll.201400384

  28. Aghaie, E., Pazouki, M., Hosseini, M.R., Ranjbar, M.: Kinetic modeling of the bioleaching process of iron removal from kaolin. Appl. Clay Sci. 65–66, 43–47 (2012). https://doi.org/10.1016/j.clay.2012.04.011

    Article  Google Scholar 

  29. Tuncuk, A., Ciftlik, S., Akcil, A.: Factorial experiments for iron removal from kaolin by using single and two-step leaching with sulfuric acid. Hydrometallurgy 134–135, 80–86 (2013). https://doi.org/10.1016/j.hydromet.2013.02.006

    Article  Google Scholar 

  30. Sun, L.X., Zhang, X., Tan, W.S., Zhu, M.L.: Effect of agitation intensity on the biooxidation process of refractory gold ores by Acidithiobacillus ferrooxidans. Hydrometallurgy 127–128, 99–103 (2012). https://doi.org/10.1016/j.hydromet.2012.07.007

    Article  Google Scholar 

  31. Zammit, C.M., Cook, N., Brugger, J., Ciobanu, C.L., Reith, F.: The future of biotechnology for gold exploration and processing. Miner. Eng. 32, 45–53 (2012). https://doi.org/10.1016/j.mineng.2012.03.016

    Article  Google Scholar 

  32. Henao, D.M.O., Godoy, M.A.M.: Jarosite pseudomorph formation from arsenopyrite oxidation using Acidithiobacillus ferrooxidans. Hydrometallurgy 104, 162–168 (2010). https://doi.org/10.1016/j.hydromet.2010.05.012

  33. Rodríguez, Y., Ballester, A., Blázquez, M.L., González, F., Muñoz, J.A.: New information on the pyrite bioleaching mechanism at low and high temperature. Hydrometallurgy 71, 37–46 (2003). https://doi.org/10.1016/S0304-386X(03)00172-5

  34. Berg, H.C., Brown, D.A.: Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239, 500–504 (1972). https://doi.org/10.1038/239500a0

  35. Berg, H.C.: E. coli in Motion. Springer, New York (2003)

    Google Scholar 

  36. Berg, H.C.: Random Walks in Biology. Princeton University Press, Princeton (1993)

    Google Scholar 

  37. Janssen, P.J.A., Graham, M.D.: Coexistence of tight and loose bundled states in a model of bacterial flagellar dynamics. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 84, 1–9 (2011). https://doi.org/10.1103/PhysRevE.84.011910

    Article  Google Scholar 

  38. Copeland, M.F., Weibel, D.B.: Bacterial swarming: a model system for studying dynamic self-assembly. Soft Matter 5, 1174 (2009). https://doi.org/10.1039/b812146j

    Article  ADS  Google Scholar 

  39. Suzuki, I., Lee, D., Mackay, B., Harahuc, L.: Effect of various ions, pH, and osmotic pressure on oxidation of elemental sulfur by Thiobacillus thiooxidans effect of various ions, pH, and osmotic pressure on oxidation of elemental sulfur by Thiobacillus thiooxidans. Appl. Environ. Microbiol. 65, 5163–5168 (1999)

    Google Scholar 

  40. Kearns, D.B.: A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8, 634–644 (2010). https://doi.org/10.1038/nrmicro2405

    Article  Google Scholar 

  41. Amouric, A., Brochier-Armanet, C., Johnson, D.B., Bonnefoy, V., Hallberg, K.B.: 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, 111–122 (2011). https://doi.org/10.1099/mic.0.044537-0

    Article  Google Scholar 

  42. Patteson, A.E., Gopinath, A., Goulian, M., Arratia, P.E.: Running and tumbling with E. coli in polymeric solutions. Sci. Rep. 5, 1–11 (2015). https://doi.org/10.1038/srep15761

    Article  Google Scholar 

  43. Mendelson, N.H., Bourque, A., Wilkening, K., Anderson, K.R., Watkins, J.C.: Organized cell swimming motions in Bacillus subtilis colonies: patterns of short-lived whirls and jets. J. Bacteriol. 181, 600–609 (1999)

    Google Scholar 

  44. Leptos, K.C., Guasto, J.S., Gollub, J.P., Pesci, A.I., Goldstein, R.E.: Dynamics of enhanced tracer diffusion in suspensions of swimming eukaryotic microorganisms. Phys. Rev. Lett. 103, (2009). https://doi.org/10.1103/PhysRevLett.103.198103

  45. Sokolov, A., Aranson, I.S.: Reduction of viscosity in suspension of swimming bacteria. Phys. Rev. Lett. 103, 2–5 (2009). https://doi.org/10.1103/PhysRevLett.103.148101

    Google Scholar 

  46. Sand, W., Gehrke, T., Jozsa, P.G., Schippers, A.: (Bio)chemistry of bacterial leaching - direct vs. indirect bioleaching. Hydrometallurgy 59, 159–175 (2001). https://doi.org/10.1016/S0304-386X(00)00180-8

  47. Ponce, J.S., Moinier, D., Byrne, D., Amouric, A., Bonnefoy, V.: 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 (2012). https://doi.org/10.1016/j.hydromet.2012.07.016

    Article  Google Scholar 

  48. Suzuki, I., Takeuchi, T.L., Yuthasastrakosol, T.D., Oh, J.K.: 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 ferrous iron and sulfur oxidation and ferric iron reduction activities of Thiobacillus f. Appl. Environ. Microbiol. 56, 1620–1626 (1990)

  49. Tributsch, H.: Direct versus indirect bioleaching. Hydrometallurgy 59, 177–185 (2001). https://doi.org/10.1016/S0304-386X(00)00181-X

    Article  Google Scholar 

  50. Caicedo, G., Prada, M., Pelaez, H., Moreno, C., Marquez, M.: Evaluation of a coal biodesulfurization process (semi-continuous mode) on the pilot plant level. Dyna 79, 114–118 (2012)

    Google Scholar 

  51. Márquez, M.A., Ospina, J.D., Morales, A.L.: New insights about the bacterial oxidation of arsenopyrite: a mineralogical scope. Miner. Eng. 39, 248–254 (2012). https://doi.org/10.1016/j.mineng.2012.06.012

    Article  Google Scholar 

  52. Mousavi, S.M., Yaghmaei, S., Salimi, F., Jafari, A.: Influence of process variables on biooxidation of ferrous sulfate by an indigenous Acidithiobacillus ferrooxidans. Part I: flask experiments. Fuel 85, 2555–2560 (2006). https://doi.org/10.1016/j.fuel.2006.05.020

    Article  Google Scholar 

  53. Ohmura, N., Tsugita, K., Koizumi, J.I., Saika, H.: Sulfur-binding protein of flagella of Thiobacillus ferrooxidans. J. Bacteriol. 178, 5776–5780 (1996)

    Article  Google Scholar 

  54. Li, Y., Li, H.: Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J. Basic Microbiol. 53, 1–6 (2013). https://doi.org/10.1002/jobm.201200300

    Article  Google Scholar 

  55. Li, Y.-Q., Wan, D.-S., Huang, S.-S., Leng, F.-F., Yan, L., Ni, Y.-Q., Li, H.-Y.: Type IV pili of Acidithiobacillus ferrooxidans are necessary for sliding, twitching motility, and adherence. Curr. Microbiol. 60, 17–24 (2010). https://doi.org/10.1007/s00284-009-9494-8

    Article  Google Scholar 

  56. Jerez, C.A.: The use of genomics, proteomics and other OMICS technologies for the global understanding of biomining microorganisms. Hydrometallurgy 94, 162–169 (2008). https://doi.org/10.1016/j.hydromet.2008.05.032

    Article  Google Scholar 

  57. Valdés, J., Pedroso, I., Quatrini, R., Dodson, R.J., Tettelin, H., Blake, R., Eisen, J.A., Holmes, D.S.: Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9, 597 (2008). https://doi.org/10.1186/1471-2164-9-597

    Article  Google Scholar 

  58. Klingl, A., Moissl-Eichinger, C., Wanner, G., Zweck, J., Huber, H., Thomm, M., Rachel, R.: Analysis of the surface proteins of Acidithiobacillus ferrooxidans strain SP5/1 and the new, pyrite-oxidizing Acidithiobacillus isolate HV2/2, and their possible involvement in pyrite oxidation. Arch. Microbiol. 193, 867–882 (2011). https://doi.org/10.1007/s00203-011-0720-y

    Article  Google Scholar 

  59. DiSPIRITO, A., Silver, M., Voss, L., Tuovinen, O.: Flagella and pili of iron-oxidizing Thiobacilli isolated from uranium mine in northern Ontario, Canada. Appl. Environ. Microbiol. 43, 1196–1200 (1982)

    Google Scholar 

  60. Silverman, M.P., Lundgren, D.G.: Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans. I. an improved medium and a harvesting procedure for securing high cell yields. J. Bacteriol. 77, 642–647 (1959)

    Google Scholar 

  61. Nemati, M., Harrison, S.T.L., Hansford, G.S., Webb, C.: Biological oxidation of ferrous sulphate by Thiobacillus ferrooxidans: a review on the kinetic aspects. Biochem. Eng. J. 1, 171–190 (1998). https://doi.org/10.1016/S1369-703X(98)00006-0

    Article  Google Scholar 

  62. Štyriaková, I., Bekényiová, A., Štyriaková, D., Jablonovská, K., Štyriak, I.: Second pilot-plant bioleaching verification of the iron removal from quartz sands. Procedia Earth Planet. Sci. 15, 861–865 (2015). https://doi.org/10.1016/j.proeps.2015.08.138

    Article  ADS  Google Scholar 

  63. Chang, R., Goldsby, K.A.: General chemistry: the essential concepts. McGraw-Hill Education - New York, New York (2014)

    Google Scholar 

  64. Refait, P., Bon, C., Simon, L., Bourrié, G., Trolard, F., Bessiére, J., Génin, J.-M.R.: Chemical composition and Gibbs standard free energy of formation of Fe(II)-Fe(III) hydroxysulphate green rust and Fe(II) hydroxide. Clay Miner. 34, 499–499 (1999). https://doi.org/10.1180/000985599546280

    Article  ADS  Google Scholar 

  65. Majzlan, J., Navrotsky, A., McCleskey, R.B., Alpers, C.N.: Thermodynamic properties and crystal structure refinement of ferricopiapite, coquimbite, rhomboclase, and F2(SO4)3(H2O)5. Eur. J. Mineral. 18, 175–186 (2006). https://doi.org/10.1127/0935-1221/2006/0018-0175

    Article  ADS  Google Scholar 

  66. Plumb, J.J., Muddle, R., Franzmann, P.D.: Effect of pH on rates of iron and sulfur oxidation by bioleaching organisms. Miner. Eng. 21, 76–82 (2008). https://doi.org/10.1016/j.mineng.2007.08.018

    Article  Google Scholar 

  67. Majzlan, J., Navrotsky, A., Schwertmann, U.: Thermodynamics of iron oxides: part III. Enthalpies of formation and stability of ferrihydrite (∼Fe(OH)3), schwertmannite (∼FeO(OH)3/4(SO4)1/8), and ε-Fe2O3. Geochim. Cosmochim. Acta 68, 1049–1059 (2004). https://doi.org/10.1016/S0016-7037(03)00371-5

  68. Brock, T.D., Gustafson, J.: Ferric iron reduction by sulfur- and iron-oxidizing bacteria. Appl. Environ. Microbiol. 32, 567–571 (1976)

    Google Scholar 

  69. Schrader, J.A., Holmes, D.S.: Phenotypic switching of Thiobacillus ferrooxidans. J. Bacteriol. 170, 3915–3923 (1988). https://doi.org/10.1128/jb.170.9.3915-3923.1988

    Article  Google Scholar 

  70. Valdés, J., Pedroso, I., Quatrini, R., Holmes, D.S.: Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: insights into their metabolism and ecophysiology. Hydrometallurgy 94, 180–184 (2008). https://doi.org/10.1016/j.hydromet.2008.05.039

  71. Abràmoff, M.D., Magalhães, P.J., Ram, S.J.: Image processing with ImageJ. Biophoton. Int. 11, 36–42 (2004)

  72. Douarche, C., Buguin, A., Salman, H., Libchaber, A.: E. coli and oxygen: a motility transition. Phys. Rev. Lett. 102, 2–5 (2009). https://doi.org/10.1103/PhysRevLett.102.198101

    Article  Google Scholar 

  73. Wu, X.L., Libchaber, A.: Particle diffusion in a quasi-two-dimensional bacterial bath. Phys. Rev. Lett. 84, 3017–3020 (2000). https://doi.org/10.1103/PhysRevLett.84.3017

    Article  ADS  Google Scholar 

  74. Miño, G., Mallouk, T.E., Darnige, T., Hoyos, M., Dauchet, J., Dunstan, J., Soto, R., Wang, Y., Rousselet, A., Clement, E.: Enhanced diffusion due to active swimmers at a solid surface. Phys. Rev. Lett. 106, 1–4 (2011). https://doi.org/10.1103/PhysRevLett.106.048102

    Article  Google Scholar 

  75. Cisneros, L.H., Cortez, R., Dombrowski, C., Goldstein, R.E., Kessler, J.O.: Fluid dynamics of self-propelled microorganisms, from individuals to concentrated populations. In: Taylor, G.K., Triantafyllou, M.S., Tropea, C. (eds.) Animal Locomotion, pp. 99–115. Springer, Berlin, Heidelberg (2010)

  76. Rice, E.W., Baird, R.B., Eaton, A.D., Clesceri, L.S.: Standard Methods for the Examination of Water and Wastewater. American Public Health Association, American Water Works Association, Water Environment Federation, Washington DC (1998)

    Google Scholar 

  77. Zhang, C., Zhang, R., Xia, J., Zhang, Q., Nie, Z.: Sulfur activation-related extracellular proteins of Acidithiobacillus ferrooxidans. Trans. Nonferrous Metals Soc. China 18, 1398–1402 (2008). https://doi.org/10.1016/S1003-6326(09)60015-7

    Article  Google Scholar 

  78. Ramírez, P., Guiliani, N., Valenzuela, L., Beard, S., Jerez, C.A.: Differential protein expression during growth of Acidithiobacillus ferrooxidans on ferrous iron, sulfur compounds, or metal sulfides. Appl. Environ. Microbiol. 70, 4491–4498 (2004). https://doi.org/10.1128/AEM.70.8.4491

    Article  Google Scholar 

  79. Yarzábal, 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 150, 2113–2123 (2004). https://doi.org/10.1099/mic.0.26966-0

    Article  Google Scholar 

  80. Sharma, P.K., Das, A., Hanumantha Rao, K., Forssberg, K.S.E.: Surface characterization of Acidithiobacillus ferrooxidans cells grown under different conditions. Hydrometallurgy 71, 285–292 (2003). https://doi.org/10.1016/S0304-386X(03)00167-1

    Article  Google Scholar 

  81. Harrison, A.P., Jarvis, B.W., Johnson, J.L.: Heterotrophic bacteria from cultures of autotrophic Thiobacillus ferrooxidans: relationships as studied by means of deoxyribonucleic acid homology. J. Bacteriol. 143, 448–454 (1980)

    Google Scholar 

  82. Son, K., Guasto, J.S., Stocker, R.: Bacteria can exploit a flagellar buckling instability to change direction. Nat. Phys. 9, 494–498 (2013). https://doi.org/10.1038/nphys2676

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial support from the Universidad Nacional de Colombia and its Faculty of Mines. They are also grateful to the Biological Hydro-Metallurgy Laboratory at the Faculty of Mines, part of the Material Characterization Laboratory, at the Universidad Nacional de Colombia, Sede Medellín. This research is embedded in the UW-Madison/UN/Ruta N agreement for the Colombia/Wisconsin One-Health Consortium at the Universidad Nacional de Colombia.

Author information

Authors and Affiliations

  1. Departamento de Materiales y Minerales, Universidad Nacional de Colombia, Sede Medellín, Calle 75 # 79A-51, Bloque M17, Faculty of Mines, Medellín, Colombia, 050034

    Juan D. Torrenegra, Liliam C. Agudelo-Morimitsu, Marco A. Márquez-Godoy & Juan P. Hernández-Ortiz

  2. Colombia/Wisconsin One-Health Consortium, Universidad Nacional de Colombia, Sede Medellín, Medellín, Colombia, 050034

    Juan D. Torrenegra, Liliam C. Agudelo-Morimitsu & Juan P. Hernández-Ortiz

  3. The Biotechnology Center, University of Wisconsin–Madison, Madison, WI, 53706-1691, USA

    Juan P. Hernández-Ortiz

Authors
  1. Juan D. Torrenegra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liliam C. Agudelo-Morimitsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marco A. Márquez-Godoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan P. Hernández-Ortiz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan P. Hernández-Ortiz.

Ethics declarations

Conflict of interest

All the authors declare that they have no conflicts of interest.

Research involving human and animal rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Torrenegra, J.D., Agudelo-Morimitsu, L.C., Márquez-Godoy, M.A. et al. Active fluid with Acidithiobacillus ferrooxidans: correlations between swimming and the oxidation route. J Biol Phys 45, 193–211 (2019). https://doi.org/10.1007/s10867-019-09524-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-019-09524-6

Keywords

Search

Navigation