Membrane vesicles as a novel strategy for shedding encrusted cell surfaces

Minerals

Volumn 4, Issue 1, 2014, Pages 74-88

  Shao, Paul P ^a   Comolli, Luis R ^b   Bernier Latmani, Rizl ^a  

^a EPFL   (Switzerland)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Biomineralization; Cryo microscopy; Detoxification; Spectro microscopy; Uranium

Indexed keywords

EID: 84930015798     PISSN: None     EISSN: 2075163X     Source Type: Journal    
DOI: 10.3390/min4010074     Document Type: Article

References (54)

1. Miot, J.; Benzerara, K.; Obst, M.; Kappler, A.; Hegler, F.; Schadler, S.; Bouchez, C.; Guyot, F.; Morin, G. Extracellular iron biomineralization by photoautotrophic iron-oxidizing bacteria. Appl. Environ. Microb. 2009, 75, 5586-5591.
2. Schadler, S.; Burkhardt, C.; Hegler, F.; Straub, K.L.; Miot, J.; Benzerara, K.; Kappler, A. Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol. J. 2009, 26, 93-103.
3. Roden, E.E. Microbial iron-redox cycling in subsurface environments. Biochem. Soc. Trans. 2012, 40, 1249-1256.
4. Emerson, D.; Roden, E.; Twining, B.S. The microbial ferrous wheel: Iron cycling in terrestrial, freshwater, and marine environments. Front. Microbiol. 2012, 3, 383.
5. Gledhill, M.; Buck, K.N. The organic complexation of iron in the marine environment: A review. Front. Microbiol. 2012, 3, 69.
6. Tebo, B.M.; Johnson, H.A.; McCarthy, J.K.; Templeton, A.S. Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 2005, 13, 421-428.
7. Spiro, T.G.; Bargar, J.R.; Sposito, G.; Tebo, B.M. Bacteriogenic manganese oxides. Acc. Chem. Res. 2010, 43, 2-9.
8. Lovley, D.R. Environmental Microbe-Metal Interactions; ASM: Washington, DC, USA, 2000.
9. Miot, J.; Maclellan, K.; Benzerara, K.; Boisset, N. Preservation of protein globules and peptidoglycan in the mineralized cell wall of nitrate-reducing, iron(II)-oxidizing bacteria: A cryo-electron microscopy study. Geobiology 2011, 9, 459-470.
10. Chan, C.S.; Fakra, S.C.; Edwards, D.C.; Emerson, D.; Banfield, J.F. Iron oxyhydroxide mineralization on microbial extracellular polysaccharides. Geochim. Cosmochim. Acta 2009, 73, 3807-3818.
11. Hegler, F.; Schmidt, C.; Schwarz, H.; Kappler, A. Does a low-pH microenvironment around phototrophic Fe(II)-oxidizing bacteria prevent cell encrustation by Fe(III) minerals? Fems. Microbiol. Ecol. 2010, 74, 592-600.
12. Beveridge, T.J. Role of cellular design in bacterial metal accumulation and mineralization. Annu. Rev. Microbiol. 1989, 43, 147-171.
13. Saini, G.; Chan, C.S. Near-neutral surface charge and hydrophilicity prevent mineral encrustation of Fe-oxidizing micro-organisms. Geobiology 2013, 11, 191-200.
14. Shelobolina, E.S.; Coppi, M.V.; Korenevsky, A.A.; DiDonato, L.N.; Sullivan, S.A.; Konishi, H.; Xu, H.; Leang, C.; Butler, J.E.; Kim, B.C.; et al. Importance of c-type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiol. 2007, 8, 7-16.
15. Fredrickson, J.K.; Zachara, J.M.; Kennedy, D.W.; Liu, C.; Duff, M.C.; Hunter, D.B.; Dohnalkova, A. Influence of Mn oxides on the reduction of uranium(VI) by the metal-reducing bacterium Shewanella putrefaciens. Geochim. Cosmochim. Acta 2002, 66, 3247-3262.
16. Bernier-Latmani, R.; Veeramani, H.; Vecchia, E.D.; Junier, P.; Lezama-Pacheco, J.S.; Suvorova, E.I.; Sharp, J.O.; Wigginton, N.S.; Bargar, J.R. Non-uraninite products of microbial U(VI) reduction. Environ. Sci. Technol. 2010, 44, 9456-9462.
17. Bargar, J.R.; Williams, K.H.; Campbell, K.M.; Long, P.E.; Stubbs, J.E.; Suvorova, E.I.; Lezama-Pacheco, J.S.; Alessi, D.S.; Stylo, M.; Webb, S.M.; et al. Uranium redox transition pathways in acetate-amended sediments. Proc. Natl. Acad. Sci. USA 2013, 110, 4506-4511.
18. Kelly, S.D.; Kemner, K.M.; Carley, J.; Criddle, C.; Jardine, P.M.; Marsh, T.L.; Phillips, D.; Watson, D.; Wu, W.-M. Speciation of uranium in sediments before and after in situ biostimulation. Environ. Sci. Technol. 2008, 42, 1558-1564.
19. Alessi, D.S.; Uster, B.; Veeramani, H.; Suvorova, E.I.; Lezama-Pacheco, J.S.; Stubbs, J.E.; Bargar, J.R.; Bernier-Latmani, R. Quantitative separation of monomeric U(IV) from UO2 in products of U(VI) reduction. Environ. Sci. Technol. 2012, 46, 6150-6157.
20. Shao, P.P.; Comolli, L.R.; Stylo, M.; Alessi, D.S.; Bargar, J.R.; Bernier-Latmani, R. Microbial extracellular polymeric substances modulate the product of uranium biomineralization. Geobiology 2013, submitted for publication.
21. Kulp, A.; Kuehn, M.J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 2010, 64, 163-184.
22. Schwechheimer, C.; Sullivan, C.J.; Kuehn, M.J. Envelope control of outer membrane vesicle production in Gram-negative bacteria. Biochemistry 2013, 52, 3031-3040.
23. Beveridge, T.J. Structures of Gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 1999, 181, 4725-4733.
24. Inagaki, S.; Onishi, S.; Kuramitsu, H.K.; Sharma, A. Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by "Tannerella forsythia". Infect. Immun. 2006, 74, 5023-5028.
25. Grenier, D.; Mayrand, D. Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect. Immun. 1987, 55, 111-117.
26. Furuta, N.; Takeuchi, H.; Amano, A. Entry of Porphyromonas gingivalis outer membrane vesicles into epithelial cells causes cellular functional impairment. Infect. Immun. 2009, 77, 4761-4770.
27. Kesty, N.C.; Mason, K.M.; Reedy, M.; Miller, S.E.; Kuehn, M.J. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 2004, 23, 4538-4549.
28. Kolling, G.L.; Matthews, K.R. Export of virulence genes and shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl. Environ. Microbiol. 1999, 65, 1843-1848.
29. Kadurugamuwa, J.L.; Beveridge, T.J. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: A novel mechanism of enzyme secretion. J. Bacteriol. 1995, 177, 3998-4008.
30. Dubern, J.F.; Diggle, S.P. Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol. Biosyst. 2008, 4, 882-888.
31. Mashburn, L.M.; Whiteley, M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 2005, 437, 422-425.
32. Renelli, M.; Matias, V.; Lo, R.Y.; Beveridge, T.J. DNA-containing membrane vesicles of Pseudomonas aeruginosa Pao1 and their genetic transformation potential. Microbiology 2004, 150, 2161-2169.
33. Whitchurch, C.B.; Tolker-Nielsen, T.; Ragas, P.C.; Mattick, J.S. Extracellular DNA required for bacterial biofilm formation. Science 2002, 295, 1487.
34. Yonezawa, H.; Osaki, T.; Kurata, S.; Fukuda, M.; Kawakami, H.; Ochiai, K.; Hanawa, T.; Kamiya, S. Outer membrane vesicles of Helicobacter pylori TK1402 are involved in biofilm formation. BMC Microbiol 2009, 9, 197, doi:10.1186/1471-2180-9-197.
35. Schooling, S.R.; Beveridge, T.J. Membrane vesicles: An overlooked component of the matrices of biofilms. J. Bacteriol. 2006, 188, 5945-5957.
36. Tan, T.T.; Morgelin, M.; Forsgren, A.; Riesbeck, K. Haemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J. Infect. Dis. 2007, 195, 1661-1670.
37. Ciofu, O.; Beveridge, T.J.; Kadurugamuwa, J.; Walther-Rasmussen, J.; Hoiby, N. Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J. Antimicrob. Chemother. 2000, 45, 9-13.
38. McBroom, A.J.; Kuehn, M.J. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 2007, 63, 545-558.
39. Tazaki, K.; Rafiqul, I.A.; Nagai, K.; Kurihara, T. FeAs2 biomineralization on encrusted bacteria in hot springs: An ecological role of symbiotic bacteria. Can. J. Earth Sci. 2003, 40, 1725-1738.
40. Benzerara, K.; Morin, G.; Yoon, T.H.; Miot, J.; Tylisczcak, T.; Casiot, C.; Bruneel, O.; Farges, F.; Brown, G.E. Nanoscale study of as biomineralization in an acid mine drainage system. Geochim. Cosmochim. Acta 2008, 72, 3949-3963.
41. Aloisi, G.; Gloter, A.; Krueger, M.; Wallmann, K.; Guyot, F.; Zuddas, P. Nucleation of calcium carbonate on bacteria nanoglobules. Geology 2006, 34, 1017-1020.
42. Rakshe, S.; Leff, M.; Spormann, A.M. Indirect modulation of the intracellular c-Di-GMP level in Shewanella oneidensis MR-1 by MxdA. Appl. Environ. Microb. 2011, 77, 2196-2198.
43. Thormann, K.M.; Duttler, S.; Saville, R.M.; Hyodo, M.; Shukla, S.; Hayakawa, Y.; Spormann, A.M. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic Di-GMP. J. Bacteriol. 2006, 188, 2681-2691.
44. Gorby, Y.; McLean, J.; Korenevsky, A.; Rosso, K.; El-Naggar, M.Y.; Beveridge, T.J. Redox-reactive membrane vesicles produced by Shewanella. Geobiology 2008, 6, 232-241.
45. Dohnalkova, A.C.; Marshall, M.J.; Arey, B.W.; Williams, K.H.; Buck, E.C.; Fredrickson, J.K. Imaging hydrated microbial extracellular polymers: Comparative analysis by electron microscopy. Appl. Environ. Microb. 2011, 77, 1254-1262.
46. Cologgi, D.L.; Lampa-Pastirk, S.; Speers, A.M.; Kelly, S.D.; Reguera, G. Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl. Acad. Sci. USA 2011, 108, 15248-15252.
47. Bencheikh-Latmani, R.; Williams, S.M.; Haucke, L.; Criddle, C.S.; Wu, L.Y.; Zhou, J.Z.; Tebo, B.M. Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr(VI) and U(VI) reduction. Appl. Environ. Microb. 2005, 71, 7453-7460.
48. Sokolov, I.; Smith, D.S.; Henderson, G.S.; Gorby, Y.A.; Ferris, F.G. Cell surface electrochemical heterogeneity of the Fe(III)-reducing bacteria Shewanella putrefaciens. Environ. Sci. Technol. 2001, 35, 341-347.
49. Liu, C.; Zachara, J.M.; Gorby, Y.A.; Szecsody, J.E.; Brown, C.F. Microbial reduction of Fe(III) and sorption/precipitation of Fe(II) on Shewanella putrefaciens strain CN32. Environ. Sci. Technol. 2001, 35, 1385-1393.
50. Studer, D.; Graber, W.; Al-Amoudi, A.; Eggli, P. A new approach for cryofixation by high-pressure freezing. J. Microsc. 2001, 203, 285-294.
51. The Boulder Lab for 3D Electron Microscopy of Cells. Available online: http://bio3d.colorado.edu/ (accessed on 26 January 2014).
52. Kremer, J.R.; Mastronarde, D.N.; McIntosh, J.R. Computer visualization of three-dimensional image data using imod. J. Struct. Biol. 1996, 116, 71-76.
53. ImageJ. Available online: http://rsb.info.nih.gov/ij/ (accessed on 26 January 2014).
54. aXis 2000-Analysis of X-ray Images and Spectra. Available online: http://unicorn.mcmaster.ca/ aXis2000.html (accessed on 26 January 2014).