Single-cell analysis of growth and cell division of the anaerobe Desulfovibrio vulgaris hildenborough

Frontiers in Microbiology

Volumn 6, Issue DEC, 2015, Pages

  Fievet, Anouchka ^a   Ducret, Adrien ^a,c   Mignot, Tâm ^a   Valette, Odile ^a   Robert, Lydia ^b   Pardoux, Romain ^a   Dolla, Alain R ^a   Aubert, Corinne ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UMR1319 MICALIS   (France)

^c INDIANA UNIVERSITY   (United States)

Author keywords

Anaerobic bacteria; Cell division; Desulfovibrio; Oxygen stress adaptation; Sulfate reducing bacteria

Indexed keywords

ANAEROBIC GROWTH; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL DIVISION; CELL ELONGATION; CHROMOSOME SEGREGATION; DESULFOVIBRIO VULGARIS; GENETIC TRANSCRIPTION; HOMEOSTASIS; NONHUMAN; PLASMID; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE CELL ANALYSIS; TIME-LAPSE VIDEO MICROSCOPY; WESTERN BLOTTING;

EID: 84954093663     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01378     Document Type: Article

References (50)

1. Barák, I., and Wilkinson, A. J. (2007). Division site recognition in Escherichia coli and Bacillus subtilis. FEMS Microbiol. Rev. 31, 311-326. doi: 10.1111/j.1574-6976.2007.00067.x
2. Bernhardt, T. G., and de Boer, P. A. J. (2005). SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol. Cell 18, 555-564. doi: 10.1016/j.molcel.2005.04.012
3. Bi, E. F., and Lutkenhaus, J. (1991). FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164. doi: 10.1038/354161a0
4. Boberek, J. M., Stach, J., and Good, L. (2010). Genetic evidence for inhibition of bacterial division protein FtsZ by berberine. PLoS ONE 5:e13745. doi: 10.1371/journal.pone.0013745
5. Boothman, C., Hockin, S., Holmes, D. E., Gadd, G. M., and Lloyd, J. R. (2006). Molecular analysis of a sulphate-reducing consortium used to treat metal-containing effluents. Biometals Int. J. Role Met. Ions Biol. Biochem. Med. 19, 601-609. doi: 10.1007/s10534-006-0006-z
6. Camberg, J. L., Hoskins, J. R., and Wickner, S. (2009). ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics. Proc. Natl. Acad. Sci. U.S.A. 106, 10614-10619. doi: 10.1073/pnas.0904886106
7. Camberg, J. L., Hoskins, J. R., and Wickner, S. (2011). The interplay of ClpXP with the cell division machinery in Escherichia coli. J. Bacteriol. 193, 1911-1918. doi: 10.1128/JB.01317-10
8. Camberg, J. L., Viola, M. G., Rea, L., Hoskins, J. R., and Wickner, S. (2014). Location of dual sites in E. coli FtsZ important for degradation by ClpXP; one at the C-terminus and one in the disordered linker. PLoS ONE 9:e94964. doi: 10.1371/journal.pone.0094964
9. Campos, M., Surovtsev, I. V., Kato, S., Paintdakhi, A., Beltran, B., Ebmeier, S. E., et al. (2014). A constant size extension drives bacterial cell size homeostasis. Cell 159, 1433-1446. doi: 10.1016/j.cell.2014.11.022
10. Canfield, D. E., and Des Marais, D. J. (1991). Aerobic sulfate reduction in microbial mats. Science 251, 1471-1473. doi: 10.1126/science.11538266
11. Charvin, G., Oikonomou, C., and Cross, F. (2010). Long-term imaging in microfluidic devices. Methods Mol. Biol. 591, 229-242. doi: 10.1007/978-1-60761-404-3_14
12. Chen, Y., Milam, S. L., and Erickson, H. P. (2012). SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry (Mosc.) 51, 3100-3109. doi: 10.1021/bi201669d
13. Cordell, S. C., Robinson, E. J. H., and Lowe, J. (2003). Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl. Acad. Sci. U.S.A. 100, 7889-7894. doi: 10.1073/pnas.1330742100
14. Dajkovic, A., Pichoff, S., Lutkenhaus, J., and Wirtz, D. (2010). Cross-linking FtsZ polymers into coherent Z rings. Mol. Microbiol. 78, 651-668. doi: 10.1111/j.1365-2958.2010.07352.x
15. de Boer, P., Crossley, R., and Rothfield, L. (1992). The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359, 254-256. doi: 10.1038/359254a0
16. Dolla, A., Fournier, M., and Dermoun, Z. (2006). Oxygen defense in sulfate-reducing bacteria. J. Biotechnol. 126, 87-100. doi: 10.1016/j.jbiotec.2006.03.041
17. Donovan, C., Schauss, A., Krämer, R., and Bramkamp, M. (2013). Chromosome segregation impacts on cell growth and division site selection in Corynebacterium glutamicum. PLoS ONE 8:e55078. doi: 10.1371/journal.pone.0055078
18. Ducret, A., Maisonneuve, E., Notareschi, P., Grossi, A., Mignot, T., and Dukan, S. (2009). A microscope automated fluidic system to study bacterial processes in real time. PLoS ONE 4:e7282. doi: 10.1371/journal.pone.0007282
19. Erickson, H. P., Anderson, D. E., and Osawa, M. (2010). FtsZ in Bacterial Cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 74, 504-528. doi: 10.1128/MMBR.00021-10
20. Eswaramoorthy, P., Erb, M. L., Gregory, J. A., Silverman, J., Pogliano, K., Pogliano, J., et al. (2011). Cellular architecture mediates DivIVA ultrastructure and regulates min activity in Bacillus subtilis. mBio 2, e00257-e00211. doi: 10.1128/mBio.00257-11
21. Fiévet, A., My, L., Cascales, E., Ansaldi, M., Pauleta, S. R., Moura, I., et al. (2011). The anaerobe-specific orange protein complex of Desulfovibrio vulgaris hildenborough is encoded by two divergent operons coregulated by s54 and a cognate transcriptional regulator. J. Bacteriol. 193, 3207-3219. doi: 10.1128/JB.00044-11
22. Ginda, K., Bezulska, M., Ziólkiewicz, M., Dziadek, J., Zakrzewska-Czerwiñska, J., and Jakimowicz, D. (2013). ParA of Mycobacterium smegmatis co-ordinates chromosome segregation with the cell cycle and interacts with the polar growth determinant DivIVA. Mol. Microbiol. 87, 998-1012. doi: 10.1111/mmi.12146
23. Hansen, M. C., Palmer, R. J., Udsen, C., White, D. C., and Molin, S. (2001). Assessment of GFP fluorescence in cells of Streptococcus gordonii under conditions of low pH and low oxygen concentration. Microbiol. Read. Engl. 147, 1383-1391. doi: 10.1099/00221287-147-5-1383
24. Harry, E., Monahan, L., and Thompson, L. (2006). Bacterial cell division: the mechanism and its precison. Int. Rev. Cytol. 253, 27-94. doi: 10.1016/S0074-7696(06)53002-5
25. Hehl, A. B., Marti, M., and Köhler, P. (2000). Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol. Biol. Cell 11, 1789-1800. doi: 10.1091/mbc.11.5.1789
26. Jia, W., Whitehead, R. N., Griffiths, L., Dawson, C., Bai, H., Waring, R. H., et al. (2012). Diversity and distribution of sulphate-reducing bacteria in human faeces from healthy subjects and patients with inflammatory bowel disease. FEMS Immunol. Med. Microbiol. 65, 55-68. doi: 10.1111/j.1574-695X.2012.00935.x
27. Jørgensen, B. B. (1982). Mineralization of organic matter in the sea bed-the role of sulphate reduction. Nature 296, 643-645. doi: 10.1038/296643a0
28. Jun, S., and Taheri-Araghi, S. (2015). Cell-size maintenance: universal strategy revealed. Trends Microbiol. 23, 4-6. doi: 10.1016/j.tim.2014.12.001
29. Kelly, A. J., Sackett, M. J., Din, N., Quardokus, E., and Brun, Y. V. (1998). Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev. 12, 880-893. doi: 10.1101/gad.12.6.880
30. Margalit, D. N., Romberg, L., Mets, R. B., Hebert, A. M., Mitchison, T. J., Kirschner, M. W., et al. (2004). Targeting cell division: small-molecule inhibitors of FtsZ GTPase perturb cytokinetic ring assembly and induce bacterial lethality. Proc. Natl. Acad. Sci. U.S.A. 101, 11821-11826. doi: 10.1073/pnas.0404439101
31. Michel, B. (2005). After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol. 3:e255. doi: 10.1371/journal.pbio.0030255
32. Mukhopadhyay, A., Redding, A. M., Joachimiak, M. P., Arkin, A. P., Borglin, S. E., Dehal, P. S., et al. (2007). Cell-wide responses to low-oxygen exposure in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 189, 5996-6010. doi: 10.1128/JB.00368-07
33. Mussmann, M., Ishii, K., Rabus, R., and Amann, R. (2005). Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ. Microbiol. 7, 405-418. doi: 10.1111/j.1462-2920.2005.00708.x
34. Peters, P. C., Migocki, M. D., Thoni, C., and Harry, E. J. (2007). A new assembly pathway for the cytokinetic Z ring from a dynamic helical structure in vegetatively growing cells of Bacillus subtilis. Mol. Microbiol. 64, 487-499. doi: 10.1111/j.1365-2958.2007.05673.x
35. Postgate, J. R., Kent, H. M., Robson, R. L., and Chesshyre, J. A. (1984). The genomes of Desulfovibrio gigas and D. vulgaris. J. Gen. Microbiol. 130, 1597-1601. doi: 10.1099/00221287-130-7-1597
36. Ravenschlag, K., Sahm, K., Knoblauch, C., Jørgensen, B. B., and Amann, R. (2000). Community Structure, Cellular rRNA Content, and Activity of Sulfate-Reducing Bacteria in Marine Arctic Sediments. Appl. Environ. Microbiol. 66, 3592-3602. doi: 10.1128/AEM.66.8.3592-3602.2000
37. Robert, L. (2015). Size sensors in bacteria, cell cycle control, and size control. Microb. Physiol. Metab. 6, 515. doi: 10.3389/fmicb.2015.00515
38. Rothfield, L., Taghbalout, A., and Shih, Y.-L. (2005). Spatial control of bacterial division-site placement. Nat. Rev. Microbiol. 3, 959-968. doi: 10.1038/nrmicro1290
39. Sass, H., Wieringa, E., Cypionka, H., Babenzien, H. D., and Overmann, J. (1998). High genetic and physiological diversity of sulfate-reducing bacteria isolated from an oligotrophic lake sediment. Arch. Microbiol. 170, 243-251. doi: 10.1007/s002030050639
40. Sass, P., Josten, M., Famulla, K., Schiffer, G., Sahl, H.-G., Hamoen, L., et al. (2011). Antibiotic acyldepsipeptides activate ClpP peptidase to degrade the cell division protein FtsZ. Proc. Natl. Acad. Sci. U. S. A. 108, 17474-17479. doi: 10.1073/pnas.1110385108
41. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675. doi: 10.1038/nmeth.2089
42. Soifer, I., Robert, L., Barkai, N., and Amir, A. (2014). Single-cell analysis of growth in budding yeast and bacteria reveals a common size regulation strategy. Available online at: http://arxiv.org/abs/1410.4771
43. Taheri-Araghi, S., Bradde, S., Sauls, J. T., Hill, N. S., Levin, P. A., Paulsson, J., et al. (2015). Cell-size control and homeostasis in bacteria. Curr. Biol. 25, 385-391. doi: 10.1016/j.cub.2014.12.009
44. Thanbichler, M., and Shapiro, L. (2006). MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126, 147-162. doi: 10.1016/j.cell.2006.05.038
45. Thanedar, S., and Margolin, W. (2004). FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167-1173. doi: 10.1016/j.cub.2004.06.048
46. Thauer, R. K., Stackebrandt, E., and Hamilton, W. A. (2007). "Energy metabolism and phylogenetic diversity of sulphate-reducing bacteria" in Sulphate-Reducing Bacteria, 1st Edn (Cambridge: Cambridge University Press), 1-38.
47. Treuner-Lange, A., Aguiluz, K., van der Does, C., Gómez-Santos, N., Harms, A., Schumacher, D., et al. (2013). PomZ, a ParA-like protein, regulates Z-ring formation and cell division in Myxococcus xanthus. Mol. Microbiol. 87, 235-253. doi: 10.1111/mmi.12094
48. Turner, J. J., Ewald, J. C., and Skotheim, J. M. (2012). Cell size control in yeast. Curr. Biol. 22, 350-359. doi: 10.1016/j.cub.2012.02.041
49. Wu, L. J., and Errington, J. (2012). Nucleoid occlusion and bacterial cell division. Nat. Rev. Microbiol. 10, 8-12. doi: 10.1038/nrmicro2671
50. Zhou, J., He, Q., Hemme, C. L., Mukhopadhyay, A., Hillesland, K., Zhou, A., et al. (2011). How sulphate-reducing microorganisms cope with stress: lessons from systems biology. Nat. Rev. Microbiol. 9, 452-466. doi: 10.1038/nrmicro2575