Filamentation

Filamentation is the anomalous growth of certain bacteria, such as Escherichia coli, in which cells continue to elongate but do not divide (no septa formation). The cells that result from elongation without division have multiple chromosomal copies.[1] In the absence of antibiotics or other stressors, filamentation occurs at a low frequency in bacterial populations (4-8% short filaments and 0-5% long filaments in 1- to 8-hour cultures),[2] the increased cell length protecting bacteria from protozoan predation and neutrophil phagocytosis by making ingestion of the cells more difficult.[1][2][3][4] Filamentation is also a virulence factor thought to protect bacteria from antibiotics, and is associated with other aspects of bacterial virulence such as biofilm formation.[5][6] The number and length of filaments within a bacterial population increases when the bacteria are treated with various chemical and physical agents (e.g. DNA synthesis-inhibiting antibiotics, UV light).[2] Some of the key genes involved in filamentation in E. coli include sulA and minCD.[7]

A Bacillus cereus cell that has undergone filamentation following antibacterial treatment (upper electron micrograph; top right) and regularly sized cells of untreated B. cereus (lower electron micrograph)

Filament formation

Antibiotic-induced filamentation

Some peptidoglycan synthesis inhibitors (e.g. cefuroxime, ceftazidime) induce filamentation by inhibiting the penicillin binding proteins (PBPs) responsible for crosslinking peptidoglycan at the septal wall (e.g. PBP3 in E. coli and P. aeruginosa). Because the PBPs responsible for lateral wall synthesis are relatively unaffected by cefuroxime and ceftazidime, cell elongation proceeds without any cell division and filamentation is observed.[2][8]

DNA synthesis-inhibiting and DNA damaging antibiotics (e.g. metronidazole, mitomycin C, the fluoroquinolones, novobiocin) induce filamentation via the SOS response. The SOS response inhibits septum formation until the DNA can be repaired, this delay stopping the transmission of damaged DNA to progeny. Bacteria inhibit septation by synthesizing protein SulA, an FtsZ inhibitor that halts Z-ring formation, thereby stopping recruitment and activation of PBP3.[2][9] If bacteria are deprived of the nucleobase thymine by treatment with folic acid synthesis inhibitors (e.g. trimethoprim), this also disrupts DNA synthesis and induces SOS-mediated filamentation. Direct obstruction of Z-ring formation by SulA and other FtsZ inhibitors (e.g. berberine) induces filamentation too.[2][10]

Some protein synthesis inhibitors (e.g. kanamycin), RNA synthesis inhibitors (e.g. bicyclomycin) and membrane disruptors (e.g. daptomycin, polymyxin B) cause filamentation too, but these filaments are much shorter than the filaments induced by the above antibiotics.[2]

Ultraviolet light-induced filamentation

UV light damages bacterial DNA and induces filamentation via the SOS response.[2][11]

Nutrition-induced filamentation

Nutritional changes may also cause bacterial filamentation.[7] For example, if bacteria are deprived of the nucleobase thymine by starvation, this disrupts DNA synthesis and induces SOS-mediated filamentation.[2][12]

See also

References

  1. Jaimes-Lizcano YA, Hunn DD, Papadopoulos KD (April 2014). "Filamentous Escherichia coli cells swimming in tapered microcapillaries". Research in Microbiology. 165 (3): 166–74. doi:10.1016/j.resmic.2014.01.007. PMID 24566556.
  2. Cushnie TP, O'Driscoll NH, Lamb AJ (December 2016). "Morphological and ultrastructural changes in bacterial cells as an indicator of antibacterial mechanism of action". Cellular and Molecular Life Sciences. 73 (23): 4471–4492. doi:10.1007/s00018-016-2302-2. hdl:10059/2129. PMID 27392605. S2CID 2065821.
  3. Hahn MW, Höfle MG (May 1998). "Grazing Pressure by a Bacterivorous Flagellate Reverses the Relative Abundance of Comamonas acidovorans PX54 and Vibrio Strain CB5 in Chemostat Cocultures". Applied and Environmental Microbiology. 64 (5): 1910–8. doi:10.1128/AEM.64.5.1910-1918.1998. PMC 106250. PMID 9572971.
  4. Hahn MW, Moore ER, Höfle MG (January 1999). "Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla". Applied and Environmental Microbiology. 65 (1): 25–35. doi:10.1128/AEM.65.1.25-35.1999. PMC 90978. PMID 9872755.
  5. Justice SS, Hunstad DA, Cegelski L, Hultgren SJ (February 2008). "Morphological plasticity as a bacterial survival strategy". Nature Reviews. Microbiology. 6 (2): 162–8. doi:10.1038/nrmicro1820. PMID 18157153. S2CID 7247384.
  6. Fuchs BB, Eby J, Nobile CJ, El Khoury JB, Mitchell AP, Mylonakis E (June 2010). "Role of filamentation in Galleria mellonella killing by Candida albicans". Microbes and Infection. 12 (6): 488–96. doi:10.1016/j.micinf.2010.03.001. PMC 288367. PMID 20223293.
  7. Bi E, Lutkenhaus J (February 1993). "Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring". Journal of Bacteriology. 175 (4): 1118–25. doi:10.1128/jb.175.4.1118-1125.1993. PMC 193028. PMID 8432706.
  8. Spratt BG (August 1975). "Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12". Proceedings of the National Academy of Sciences of the United States of America. 72 (8): 2999–3003. Bibcode:1975PNAS...72.2999S. doi:10.1073/pnas.72.8.2999. PMC 432906. PMID 1103132.
  9. Cordell SC, Robinson EJ, Lowe J (June 2003). "Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ". Proceedings of the National Academy of Sciences of the United States of America. 100 (13): 7889–94. Bibcode:2003PNAS..100.7889C. doi:10.1073/pnas.1330742100. PMC 164683. PMID 12808143.
  10. Ray S, Dhaked HP, Panda D (October 2014). "Antimicrobial peptide CRAMP (16-33) stalls bacterial cytokinesis by inhibiting FtsZ assembly". Biochemistry. 53 (41): 6426–9. doi:10.1021/bi501115p. PMID 25294259.
  11. Walker JR, Pardee AB (January 1968). "Evidence for a relationship between deoxyribonucleic acid metabolism and septum formation in Escherichia coli". Journal of Bacteriology. 95 (1): 123–31. doi:10.1128/JB.95.1.123-131.1968. PMC 251980. PMID 4867214.
  12. Ohkawa T (December 1975). "Studies of intracellular thymidine nucleotides. Thymineless death and the recovery after re-addition of thymine in Escherichia coli K 12". European Journal of Biochemistry. 60 (1): 57–66. doi:10.1111/j.1432-1033.1975.tb20975.x. PMID 1107038.
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