Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

Force microscopy has been used to quantitatively measure the infinitesimal forces that characterize interactions between Shewanella oneidensis (a dissimilatory metal-reducing bacterium) and goethite (α-FeOOH), both commonly found in Earth near-surface environments. Force measurements with subnanonewton resolution were made in real time with living cells under aerobic and anaerobic solutions as a function of the distance, in nanometers, between a cell and the mineral surface. Energy values [in attojoules (10 −18 joules)] derived from these measurements show that the affinity between S. oneidensis and goethite rapidly increases by two to five times under anaerobic conditions in which electron transfer from bacterium to mineral is expected. Specific signatures in the force curves suggest that a 150-kilodalton putative iron reductase is mobilized within the outer membrane of S. oneidensis and specifically interacts with the goethite surface to facilitate the electron transfer process.

Bibliography

Lower, S. K., Hochella, M. F., & Beveridge, T. J. (2001). Bacterial Recognition of Mineral Surfaces: Nanoscale Interactions Between Shewanella and α-FeOOH. Science, 292(5520), 1360–1363.

Authors 3
  1. Steven K. Lower (first)
  2. Michael F. Hochella (additional)
  3. Terry J. Beveridge (additional)
References 48 Referenced 371
  1. 10.1128/mr.55.2.259-287.1991
  2. 10.1146/annurev.mi.48.100194.001523
  3. 10.1128/aem.56.9.2811-2817.1990
  4. 10.1128/jb.172.11.6232-6238.1990
  5. 10.1128/aem.52.4.751-757.1986
  6. 10.1002/bit.260320902
  7. 10.1128/aem.54.6.1472-1480.1988
  8. 10.1021/es9506216
  9. 10.1128/aem.63.10.3837-3843.1997
  10. 10.1016/S0016-7037(98)00243-9
  11. 10.2138/am-1998-11-1232
  12. 10.1021/es990447b
  13. 10.1128/jb.179.4.1143-1152.1997
  14. 10.1128/JB.182.1.67-75.2000
  15. 10.1128/jb.174.11.3429-3438.1992
  16. 10.1111/j.1574-6968.1993.tb06066.x
  17. 10.1016/S0005-2736(97)00034-5
  18. 10.1016/S0005-2736(98)00111-4
  19. 10.1016/S0016-7037(00)00430-0
  20. 10.1080/01490450151079798
  21. 10.1099/00207713-49-2-705
  22. S. oneidensis (American Type Culture Collection no. 700550) was transformed with plasmid pSMC2 which codes for a constitutive intracellular green fluorescent protein (44). Transformed cells were grown in an anaerobic chamber (Coy Laboratory Products Ann Arbor MI) to midlogarithmic phase at room temperature as previously described (4) in a defined medium supplemented with 15 mM lactate and 2 mM ferric citrate (4).
  23. Glass beads (Polysciences Warrington PA) were cleaned with hydrogen peroxide (30% solution) rinsed with ultrapure water and functionalized with amino groups by incubation in a solution of 3-aminopropyltriethoxysilane (5 to 10% in acetone) for 6 hours. Previous studies have shown that linker molecules such as amino-silane have no effect on the measured bacterium-mineral interactions (19 20). Cultured cells were rinsed three times in an anaerobic solution of 10 mM sodium chloride and were linked to functionalized glass beads by spinning the cell-bead mixture at 7000 g for 2 min. A single bacteria-coated bead was then attached to a cantilever with epoxy (19). Scanning laser confocal microscopy was used to verify bacterial coverage of the probe by imaging the green fluorescent signal emitted from cells (19 20). The viability of cells was assessed by inoculating an agar plate with a biologically active force probe after the force measurements.
  24. It is difficult to quantify the area of contact between a force probe and a sample surface. Three-dimensional confocal microscopy measurements of biologically active force probes as described previously (19 20) suggest that a single bacterium made contact with the mineral during force measurements.
  25. The region of constant compliance was not used to determine deflection because it would have resulted in an overestimate of the measured forces because of the fact that the cells were more compliant than the cantilever (20 45).
  26. 10.1063/1.1144209
  27. 10.1021/la00043a024
  28. 10.1038/35011098
  29. 10.1128/jb.176.5.1468-1474.1994
  30. 10.1128/JB.180.23.6292-6297.1998
  31. 10.1021/es001258s
  32. W. Stumm J. J. Morgan Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters (Wiley New York ed. 3 1996) pp 534–540.
  33. 10.1073/pnas.89.18.8651
  34. 10.1128/aem.59.12.4044-4050.1993
  35. 10.1128/JB.181.16.4725-4733.1999
  36. On the basis of transmission electron microscopy and freeze-substitution analyses extracellular polysaccharide a common macromolcule on the surface of many bacteria has not been detected on the cell wall of S. oneidensis (A. Korenevsky and T. Beveridge unpublished data).
  37. P. J. Flory Statistical Mechanics of Chain Molecules (Hanser New York 1989) pp. 401–403.
  38. 10.1126/science.276.5315.1109
  39. 10.1016/S0006-3495(99)77272-3
  40. 10.1073/pnas.96.23.13170
  41. J.-J. Karlsson A. Kadziola A. Rasmussen T. E. Rostrup J. Ulstrup in Protein Folds: A Distance-Based Approach H. Bohr S. Brunak Eds. (CRC Press Boca Raton FL 1996) pp. 56–67.
  42. 10.1128/AEM.67.1.260-269.2001
  43. Future studies will use biological force microscopy with mutants incapable of producing and/or secreting cell wall biomolecules such as the 150-kD protein.
  44. G. V. Bloemberg G. A. O'Toole
  45. 10.1128/aem.63.11.4543-4551.1997
  46. N. P. D'Costa
  47. 10.1063/1.1146135
  48. We thank B. Lower C. Myers J. Banfield and the anonymous reviewers for constructive comments; G. O'Toole for providing plasmid pSMC2; and J. Tak for support. This manuscript is dedicated to B. Diehl. Mineral samples were provided by the Virginia Tech Geological Sciences Museum. Financial support was provided by the U.S. Department of Energy and the NSF.
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 1:52 a.m.)
Deposited 1 year, 7 months ago (Jan. 9, 2024, 12:19 p.m.)
Indexed 1 week, 2 days ago (Aug. 28, 2025, 8:07 a.m.)
Issued 24 years, 3 months ago (May 18, 2001)
Published 24 years, 3 months ago (May 18, 2001)
Published Print 24 years, 3 months ago (May 18, 2001)
Funders 0

None

@article{Lower_2001, title={Bacterial Recognition of Mineral Surfaces: Nanoscale Interactions Between Shewanella and α-FeOOH}, volume={292}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.1059567}, DOI={10.1126/science.1059567}, number={5520}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Lower, Steven K. and Hochella, Michael F. and Beveridge, Terry J.}, year={2001}, month=may, pages={1360–1363} }