Biological consequences and advantages of asymmetric bacterial growth

Annual Review of Microbiology

Volumn 67, Issue , 2013, Pages 417-435

  Kysela, David T ^a   Brown, Pamela J B ^b   Huang, Kerwyn Casey ^c,d   Brun, Yves V ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c Stanford University   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Asymmetry; Damage; Peptidoglycan; Sporulation

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA; MESSENGER RNA; MREB PROTEIN; PEPTIDOGLYCAN;

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; ARTICLE; ASYMMETRIC CELL DIVISION; ASYMMETRIC SYNTHESIS; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIAL SURVIVAL; BIOFILM; CAULOBACTER CRESCENTUS; CELL AGING; CELL DAMAGE; CELL ELONGATION; CELL GROWTH; CELL POLARITY; CELL SHAPE; CELLULAR DISTRIBUTION; DAUGHTER CELL; ENVIRONMENTAL CHANGE; ESCHERICHIA COLI; EUKARYOTE EVOLUTION; GENETIC VARIABILITY; NONHUMAN; NUTRIENT LIMITATION; PHENOTYPIC PLASTICITY; PHENOTYPIC VARIATION; PLEIOTROPY; POLAR BODY; PRIORITY JOURNAL; RHIZOBIUM RADIOBACTER; RHODOPSEUDOMONAS; SPOROGENESIS; STAPHYLOCOCCUS AUREUS; STREPTOMYCES;

BACTERIA; CELL DIVISION; PHYLOGENY;

EID: 84884517569     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092412-155622     Document Type: Article

References (98)

1. AaronM, Charbon G, LamH, Schwarz H, Vollmer W, Jacobs-WagnerC. 2007. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol. Microbiol. 64:938-52
2. Ackermann M, Chao L, Bergstrom CT, Doebeli M. 2007. On the evolutionary origin of aging. Aging Cell 6:235-44
3. AckermannM, Schauerte A, Stearns SC, Jenal U. 2007. Experimental evolution of aging in a bacterium. BMC Evol. Biol. 7:126
4. Ackermann M, Stearns SC, Jenal U. 2003. Senescence in a bacterium with asymmetric division. Science 300:1920
5. Aguilaniu H, Gustafsson L, Rigoulet M, Nyström T. 2003. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299:1751-53
6. Aldridge BB, Fernandez-Suarez M, Heller D, Ambravaneswaran V, Irimia D, et al. 2012. Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 335:100-4
7. Barker MG, Walmsley RM. 1999. Replicative ageing in the fission yeast Schizosaccharomyces pombe. Yeast 15:1511-18
8. Ben-Yehuda S, Losick R. 2002. Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109:257-66
9. Berne C, Kysela DT, Brun YV. 2010. A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Mol. Microbiol. 77:815-29
10. Bowman GR, Lyuksyutova AI, Shapiro L. 2011. Bacterial polarity. Curr. Opin. Cell Biol. 23:71-77
11. Brilli M, Fondi M, Fani R, Mengoni A, Ferri L, et al. 2010. The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Syst. Biol. 4:52
12. Brown PJ, de Pedro MA, Kysela DT, Van der Henst C, Kim J, et al. 2012. Polar growth in the alphaproteobacterial order Rhizobiales. Proc. Natl. Acad. Sci. USA 109:1697-701
13. Chao L. 2010. A model for damage load and its implications for the evolution of bacterial aging. PLoS Genet. pii:e1001076
14. Chauhan A, LoftonH, Maloney E, Moore J, Fol M, et al. 2006. Interference of Mycobacterium tuberculosis cell division by Rv2719c, a cell wall hydrolase. Mol. Microbiol. 62:132-47
15. Christen M, Kulasekara HD, Christen B, Kulasekara BR, Hoffman LR, Miller SI. 2010. Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 328:1295-97
16. Curtis PD, Brun YV. 2010. Getting in the loop: regulation of development in Caulobacter crescentus. Microbiol. Mol. Biol. Rev. 74:13-41
17. Daniel RA, Errington J. 2003. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767-76
18. de PedroMA, Grunfelder CG, Schwarz H. 2004. Restricted mobility of cell surface proteins in the polar regions of Escherichia coli. J. Bacteriol. 186:2594-602
19. de PedroMA, Quintela JC, Holtje JV, SchwarzH. 1997. Murein segregation in Escherichia coli. J. Bacteriol. 179:2823-34
20. den Blaauwen T, de Pedro MA, Nguyen-Disteche M, Ayala JA. 2008. Morphogenesis of rod-shaped sacculi. FEMS Microbiol. Rev. 32:321-44
21. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, Carballido-Lopez R. 2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:225-28
22. Dougherty TJ, Kennedy K, Kessler RE, Pucci MJ. 1996. Direct quantitation of the number of individual penicillin-binding proteins per cell in Escherichia coli. J. Bacteriol. 178:6110-15
23. Eichenberger P, Fawcett P, Losick R. 2001. A three-protein inhibitor of polar septation during sporulation in Bacillus subtilis. Mol. Microbiol. 42:1147-62
24. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297:1183-86
25. Entcheva-Dimitrov P, Spormann AM. 2004. Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus. J. Bacteriol. 186:8254-66
26. Erjavec N, Cvijovic M, KlippE, NyströmT. 2008. Selective benefits of damage partitioning in unicellular systems and its effects on aging. Proc. Natl. Acad. Sci. USA 105:18764-69
27. Errington J. 2003. Regulation of endospore formation in Bacillus subtilis. Nat. Rev. Microbiol. 1:117-26
28. Evans SN, SteinsaltzD. 2007. Damage segregation at fissioningmay increase growth rates: a superprocess model. Theor. Popul. Biol. 71:473-90
29. Fisher RA. 1958. The Genetical Theory of Natural Selection. New York: Dover. 291 pp.
30. Flardh K. 2003. Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol. Microbiol. 49:1523-36
31. Flardh K. 2003. Growth polarity and cell division in Streptomyces. Curr. Opin. Microbiol. 6:564-71
32. Flardh K. 2010. Cell polarity and the control of apical growth in Streptomyces. Curr. Opin. Microbiol. 13:758-65
33. Flardh K, Richards DM, Hempel AM, Howard M, Buttner MJ. 2012. Regulation of apical growth and hyphal branching in Streptomyces. Curr. Opin. Microbiol. 15:737-43
34. Furchtgott L, Wingreen NS, Huang KC. 2011. Mechanisms for maintaining cell shape in rod-shaped gram-negative bacteria. Mol. Microbiol. 81:340-53
35. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:222-25
36. Gitai Z. 2005. The new bacterial cell biology:moving parts and subcellular architecture. Cell 120:577-86
37. Gorke B, Stulke J. 2008. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat. Rev. Microbiol. 6:613-24
38. Hallatschek O, Hersen P, Ramanathan S, Nelson DR. 2007. Genetic drift at expanding frontiers promotes gene segregation. Proc. Natl. Acad. Sci. USA 104:19926-30
39. Hallez R, Bellefontaine AF, Letesson JJ, De Bolle X. 2004. Morphological and functional asymmetry in alpha-proteobacteria. Trends Microbiol. 12:361-65
40. Hastings A. 1997. Population Biology: Concepts and Models. New York: Springer. 220 pp.
41. Hempel AM, Cantlay S, Molle V, Wang SB, Naldrett MJ, et al. 2012. The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc. Natl. Acad. Sci. USA 109:E2371-79
42. Higgins D, Dworkin J. 2012. Recent progress in Bacillus subtilis sporulation.FEMS Microbiol. Rev. 36:131-48
43. Hirsch P. 1974. Budding bacteria. Annu. Rev. Microbiol. 28:391-444
44. Holtje JV. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203
45. Huang HC, Ehrhardt DW, Shaevitz JW. 2012. The molecular origins of chiral growth in walled cells. Curr. Opin. Microbiol. 15:1-8
46. Joyce G, Williams KJ, Robb M, Noens E, Tizzano B, et al. 2012. Cell division site placement and asymmetric growth in mycobacteria. PLoS ONE 7:e44582
47. Kang CM, Nyayapathy S, Lee JY, Suh JW, Husson RN. 2008. Wag31, a homologue of the cell division proteinDivIVA, regulates growth, morphology and polar cell wall synthesis inmycobacteria. Microbiology 154:725-35
48. Kaval KG, Halbedel S. 2012. Architecturally the same, but playing a different game: the diverse speciesspecific roles of DivIVA proteins. Virulence 3:406-7
49. Kirkpatrick CL, Viollier PH. 2011. Poles apart: prokaryotic polar organelles and their spatial regulation. Cold Spring Harb. Perspect. Biol. 3:a006809
50. Kocaoglu O, Calvo RA, Sham LT, Cozy LM, Lanning BR, et al. 2012. Selective penicillin-binding protein imaging probes reveal substructure in bacterial cell division. ACS Chem. Biol. 7:1746-53
51. Kuru E, Hughes HV, Brown PJ, Hall E, Tekkam S, et al. 2012. In situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew. Chem. Int. Ed. Engl. 51:12519-23
52. Letek M, Fiuza M, Ordonez E, Villadangos AF, Flardh K, et al. 2009. DivIVA uses an N-terminal conserved region and two coiled-coil domains to localize and sustain the polar growth in Corynebacterium glutamicum. FEMS Microbiol. Lett. 297:110-16
53. Levins R. 1968. Evolution in Changing Environments: Some Theoretical Explorations. Princeton, NJ:Princeton Univ. Press. 120 pp.
54. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, et al. 2012. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol. Microbiol. 83:41-51
55. Lindner AB, Madden R, Demarez A, Stewart EJ, Taddei F. 2008. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl. Acad. Sci. USA 105:3076-81
56. Lucet I, Feucht A, Yudkin MD, Errington J. 2000. Direct interaction between the cell division protein FtsZ and the cell differentiation protein SpoIIE. EMBO J. 19:1467-75
57. Macara IG, Mili S. 2008. Polarity and differential inheritance-universal attributes of life? Cell 135:801-12
58. Margolin W. 2009. Sculpting the bacterial cell. Curr. Biol. 19:R812-22
59. Mazza P, Noens EE, Schirner K, Grantcharova N, Mommaas AM, et al. 2006. MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol. Microbiol. 60:838-52
60. Medawar PB. 1957. An unsolved problem of biology. In Uniqueness of the Individual, ed. PB Medawar, pp. 44-70. London: Methuen
61. Meyers LA, Bull JJ. 2002. Fighting change with change: adaptive variation in an uncertain world. Trends Ecol. Evol 17:551-57
62. Moore RL. 1981. The biology of Hyphomicrobium and other prosthecate, budding bacteria. Annu. Rev. Microbiol. 35:567-94
63. Moore RL. 1981. The genera Hyphomicrobium, Pedomicrobium, and Hyphomonas. In The Prokaryotes: A Handbook on Habitats, Isolation, and Identification of Bacteria, ed.MPStarr, HStolp, HGTrüper, A Balows, HG Schlegel, pp. 480-87. Berlin/New York: Springer
64. Moore RL, Hirsch P. 1973. First generation synchrony of isolated Hyphomicrobium swarmer populations. J. Bacteriol. 116:418-23
65. Mortimer RK, Johnston JR. 1959. Life span of individual yeast cells. Nature 183:1751-52
66. Neumuller RA, Knoblich JA. 2009. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23:2675-99
67. Partridge L, Barton NH. 1993. Optimality, mutation and the evolution of ageing. Nature 362:305-11
68. Pogliano J, Osborne N, Sharp MD, Abanes-De Mello A, Perez A, et al. 1999. A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol. Microbiol. 31:1149-59
69. Poindexter JS. 1981. The caulobacters: ubiquitous unusual bacteria. Microbiol. Rev. 45:123-79
70. Poindexter JS, Pujara KP, Staley JT. 2000. In situ reproductive rate of freshwater Caulobacter spp. Appl. Environ. Microbiol. 66:4105-11
71. Potluri LP, Kannan S, Young KD. 2012. ZipA is required for FtsZ-dependent preseptal peptidoglycan synthesis prior to invagination during cell division. J. Bacteriol. 194:5334-42
72. Rang CU, Peng AY, Chao L. 2011. Temporal dynamics of bacterial aging and rejuvenation. Curr. Biol. 21:1813-16
73. Rang CU, Peng AY, Poon AF, Chao L. 2012. Ageing in Escherichia coli requires damage by an extrinsic agent. Microbiology 158:1553-59
74. Richards DM, Hempel AM, Flardh K, Buttner MJ, Howard M. 2012. Mechanistic basis of branch-site selection in filamentous bacteria. PLoS Comput. Biol. 8:e1002423
75. Rose MR. 1991. Evolutionary Biology of Aging. New York: Oxford Univ. Press. 221 pp.
76. Scheffers DJ, Pinho MG. 2005. Bacterial cell wall synthesis: new insights from localization studies. Microbiol. Mol. Biol. Rev. 69:585-607
77. Shapiro L, McAdams HH, Losick R. 2002. Generating and exploiting polarity in bacteria. Science 298:1942-46
78. Sharma R, Peacock L, Gluenz E, Gull K, Gibson W, Carrington M. 2008. Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. Protist 159:137-51
79. Staley JT. 1968. Prosthecomicrobium and Ancalomicrobium: new prosthecate freshwater bacteria. J. Bacteriol. 95:1921-42
80. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-90
81. Stewart EJ, Madden R, Paul G, Taddei F. 2005. Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol. 3:e45
82. Storz G, Hengge R, American Society for Microbiology. 2011. Bacterial Stress Responses. Washington, DC: ASM Press. 506 pp.
83. Tajbakhsh S, Rocheteau P, Le Roux I. 2009. Asymmetric cell divisions and asymmetric cell fates. Annu. Rev. Cell Dev. Biol. 25:671-99
84. Travis JMJ, Dytham C. 1998. The evolution of dispersal in a metapopulation: a spatially explicit, individual-based model. Proc. R. Soc. B Biol. Sci. 265:17-23
85. Tsokos CG, Laub MT. 2012. Polarity and cell fate asymmetry in Caulobacter crescentus. Curr. Opin. Microbiol. 15:744-50
86. Typas A, Banzhaf M, Gross CA, Vollmer W. 2012. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10:123-36
87. Tzagoloff H, Novick R. 1977. Geometry of cell division in Staphylococcus aureus. J. Bacteriol. 129:343-50
88. Ursell TS, Trepagnier EH, Huang KC, Theriot JA. 2012. Analysis of surface protein expression reveals the growth pattern of the gram-negative outer membrane. PLoS Comput. Biol. 8:e1002680
89. van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS, et al. 2011. The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc. Natl. Acad. Sci. USA 108:15822-27
90. Veening JW, Stewart EJ, Berngruber TW, Taddei F, Kuipers OP, Hamoen LW. 2008. Bet-hedging and epigenetic inheritance in bacterial cell development. Proc. Natl. Acad. Sci. USA 105:4393-98
91. Vollmer W, Blanot D, de Pedro MA. 2008. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32:149-67
92. Wagner-Herman JK, Bernard R, Dunne R, Bisson-Filho AW, Kumar K, et al. 2012. RefZ facilitates the switch from medial to polar division during spore formation in Bacillus subtilis. J. Bacteriol. 194:4608-18
93. Wali TM, Hudson GR, Danald DA, Weiner RM. 1980. Timing of swarmer cell cycle morphogenesis and macromolecular synthesis by Hyphomicrobium neptunium in synchronous culture. J. Bacteriol. 144:406-12
94. Wang S, Furchtgott L, Huang KC, Shaevitz JW. 2012. Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall. Proc. Natl. Acad. Sci. USA 109:E595-604
95. White CL, Gober JW. 2012. MreB: pilot or passenger of cell wall synthesis? Trends Microbiol. 20:74-79
96. Whittenbury R, Dow CS. 1977. Morphogenesis and differentiation in Rhodomicrobium vannielii and other budding and prosthecate bacteria. Bacteriol. Rev. 41:754-808
97. Wientjes FB, Nanninga N. 1989. Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J. Bacteriol. 171:3412-19
98. WilliamsGC. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398-411