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Filamentation

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(Redirected from Filamentous bacteria)
For other uses, see Filament (disambiguation).
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)

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).[1][2] 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).[3] The increased cell length can protect bacteria from protozoan predation and neutrophil phagocytosis by making ingestion of cells more difficult.[1][3][4][5] Filamentation is also thought to protect bacteria from antibiotics, and is associated with other aspects of bacterial virulence such as biofilm formation.[6][7]

The number and length of filaments within a bacterial population increases when the bacteria are exposed to different physical, chemical and biological agents (e.g. UV light, DNA synthesis-inhibiting antibiotics, bacteriophages).[3][8] This is termed conditional filamentation.[2] Some of the key genes involved in filamentation in E. coli include sulA, minCD and damX.[9][10]

Filament formation

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Antibiotic-induced filamentation

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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.[3][11][12]

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.[3][13] 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.[3][14][15]

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.[3]

Stress-induced filamentation

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Filamentation is often a consequence of environmental stress. It has been observed in response to temperature shocks,[16] low water availability,[17] high osmolarity,[18] extreme pH,[19] and UV exposure.[20] UV light damages bacterial DNA and induces filamentation via the SOS response.[3][21] Starvation can also cause bacterial filamentation.[9] For example, if bacteria are deprived of the nucleobase thymine, this disrupts DNA synthesis and induces SOS-mediated filamentation.[3][22]

Nutrient-induced filamentation

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Several macronutrients and biomolecules can cause bacterial cells to filament, including the amino acids glutamine, proline and arginine, and some branched-chain amino acids.[23] Certain bacterial species, such as Paraburkholderia elongata, will also filament as a result of a tendency to accumulate phosphate in the form of polyphosphate, which can chelate metal cofactors needed by division proteins.[2] In addition, filamentation is induced by nutrient-rich conditions in the intracellular pathogen Bordetella atropi. This occurs via the highly conserved UDP-glucose pathway. UDP-glucose biosynthesis and sensing suppresses bacterial cell division, with the ensuing filamentation allowing B. atropi to spread to neighboring cells.[24]

Intrinsic dysbiosis-induced filamentation

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Filamentation can also be induced by other pathways affecting thymidylate synthesis. For instance, partial loss of dihydrofolate reductase (DHFR) activity causes reversible filamentation.[25] DHFR has a critical role in regulating the amount of tetrahydrofolate, which is essential for purine and thymidylate synthesis. DHFR activity can be inhibited by mutations or by high concentrations of the antibiotic trimethoprim (see antibiotic-induced filamentation above).

Overcrowding of the periplasm or envelope can also induce filamentation in Gram-negative bacteria by disrupting normal divisome function.[26][27]

Filamentation and biotic interactions

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Several examples of filamentation that result from biotic interactions between bacteria and other organisms or infectious agents have been reported. Filamentous cells are resistant to ingestion by bacterivores, and environmental conditions generated during predation can trigger filamentation.[28] Filamentation can also be induced by signalling factors produced by other bacteria.[29] In addition, Agrobacterium spp. filament in proximity to plant roots,[30] and E. coli filaments when exposed to plant extracts.[31] Lastly, bacteriophage infection can result in filamentation via the expression of proteins that inhibit divisome assembly.[8]

See also

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References

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  1. ^ a b c 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. ^ a b c Karasz DC, Weaver AI, Buckley DH, Wilhelm RC (January 2022). "Conditional filamentation as an adaptive trait of bacteria and its ecological significance in soils". Environmental Microbiology. 24 (1): 1–17. doi:10.1111/1462-2920.15871. OSTI 1863903. PMID 34929753. S2CID 245412965.
  3. ^ a b c d e f g h i 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.
  4. ^ 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. Bibcode:1998ApEnM..64.1910H. doi:10.1128/AEM.64.5.1910-1918.1998. PMC 106250. PMID 9572971.
  5. ^ 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. Bibcode:1999ApEnM..65...25H. doi:10.1128/AEM.65.1.25-35.1999. PMC 90978. PMID 9872755.
  6. ^ 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.
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  8. ^ a b Ragunathan PT, Vanderpool CK (December 2019). "Cryptic-Prophage-Encoded Small Protein DicB Protects Escherichia coli from Phage Infection by Inhibiting Inner Membrane Receptor Proteins". Journal of Bacteriology. 201 (23). doi:10.1128/JB.00475-19. PMC 6832061. PMID 31527115.
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  10. ^ Khandige S, Asferg CA, Rasmussen KJ, Larsen MJ, Overgaard M, Andersen TE, Møller-Jensen J (August 2016). Justice S, Hultgren SJ (eds.). "DamX Controls Reversible Cell Morphology Switching in Uropathogenic Escherichia coli". mBio. 7 (4). doi:10.1128/mBio.00642-16. PMC 4981707. PMID 27486187.
  11. ^ 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.
  12. ^ Bush K, Bradford PA (August 2016). "β-Lactams and β-Lactamase Inhibitors: An Overview". Cold Spring Harbor Perspectives in Medicine. 6 (8): a025247. doi:10.1101/cshperspect.a025247. PMC 4968164. PMID 27329032.
  13. ^ 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.
  14. ^ 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.
  15. ^ Sass P, Brötz-Oesterhelt H (October 2013). "Bacterial cell division as a target for new antibiotics". Current Opinion in Microbiology. 16 (5): 522–530. doi:10.1016/j.mib.2013.07.006. PMID 23932516.
  16. ^ Gill CO, Badoni M, Jones TH (November 2007). "Behaviours of log phase cultures of eight strains of Escherichia coli incubated at temperatures of 2, 6, 8 and 10 degrees C". International Journal of Food Microbiology. 119 (3): 200–206. doi:10.1016/j.ijfoodmicro.2007.07.043. PMID 17719669.
  17. ^ Mattick KL, Jørgensen F, Legan JD, Cole MB, Porter J, Lappin-Scott HM, Humphrey TJ (April 2000). "Survival and filamentation of Salmonella enterica serovar enteritidis PT4 and Salmonella enterica serovar typhimurium DT104 at low water activity". Applied and Environmental Microbiology. 66 (4): 1274–1279. Bibcode:2000ApEnM..66.1274M. doi:10.1128/AEM.66.4.1274-1279.2000. PMC 91980. PMID 10742199.
  18. ^ Chang WS, Halverson LJ (October 2003). "Reduced water availability influences the dynamics, development, and ultrastructural properties of Pseudomonas putida biofilms". Journal of Bacteriology. 185 (20): 6199–6204. doi:10.1128/JB.185.20.6199-6204.2003. PMC 225025. PMID 14526033.
  19. ^ Jones TH, Vail KM, McMullen LM (July 2013). "Filament formation by foodborne bacteria under sublethal stress". International Journal of Food Microbiology. 165 (2): 97–110. doi:10.1016/j.ijfoodmicro.2013.05.001. PMID 23727653.
  20. ^ Modenutti B, Balseiro E, Corno G, Callieri C, Bertoni R, Caravati E (July 2010). "Ultraviolet radiation induces filamentation in bacterial assemblages from North Andean Patagonian lakes". Photochemistry and Photobiology. 86 (4): 871–881. doi:10.1111/j.1751-1097.2010.00758.x. PMID 20528974. S2CID 45542973.
  21. ^ 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): 123–131. doi:10.1128/JB.95.1.123-131.1968. PMC 251980. PMID 4867214.
  22. ^ 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.
  23. ^ Jensen RH, Woolfolk CA (August 1985). "Formation of Filaments by Pseudomonas putida". Applied and Environmental Microbiology. 50 (2): 364–372. Bibcode:1985ApEnM..50..364J. doi:10.1128/aem.50.2.364-372.1985. PMC 238629. PMID 16346856.
  24. ^ Tran TD, Ali MA, Lee D, Félix MA, Luallen RJ (February 2022). "Bacterial filamentation as a mechanism for cell-to-cell spread within an animal host". Nature Communications. 13 (1): 693. Bibcode:2022NatCo..13..693T. doi:10.1038/s41467-022-28297-6. PMC 8816909. PMID 35121734.
  25. ^ Bhattacharyya S, Bershtein S, Adkar BV, Woodard J, Shakhnovich EI (June 2021). "Metabolic response to point mutations reveals principles of modulation of in vivo enzyme activity and phenotype". Molecular Systems Biology. 17 (6): e10200. arXiv:2012.09658. doi:10.15252/msb.202110200. PMC 8236904. PMID 34180142.
  26. ^ Lau SY, Zgurskaya HI (November 2005). "Cell division defects in Escherichia coli deficient in the multidrug efflux transporter AcrEF-TolC". Journal of Bacteriology. 187 (22): 7815–7825. doi:10.1128/JB.187.22.7815-7825.2005. PMC 1280316. PMID 16267305.
  27. ^ Gode-Potratz CJ, Kustusch RJ, Breheny PJ, Weiss DS, McCarter LL (January 2011). "Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence". Molecular Microbiology. 79 (1): 240–263. doi:10.1111/j.1365-2958.2010.07445.x. PMC 3075615. PMID 21166906.
  28. ^ Corno G, Jürgens K (January 2006). "Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity". Applied and Environmental Microbiology. 72 (1): 78–86. Bibcode:2006ApEnM..72...78C. doi:10.1128/AEM.72.1.78-86.2006. PMC 1352273. PMID 16391028.
  29. ^ Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, et al. (April 2008). "Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa". Molecular Microbiology. 68 (1): 75–86. doi:10.1111/j.1365-2958.2008.06132.x. PMID 18312265. S2CID 26725907.
  30. ^ Finer KR, Larkin KM, Martin BJ, Finer JJ (February 2001). "Proximity of Agrobacterium to living plant tissues induces conversion to a filamentous bacterial form". Plant Cell Reports. 20 (3): 250–255. doi:10.1007/s002990100315. S2CID 24531530.
  31. ^ Mohamed-Salem R, Rodríguez Fernández C, Nieto-Pelegrín E, Conde-Valentín B, Rumbero A, Martinez-Quiles N (2019). "Aqueous extract of Hibiscus sabdariffa inhibits pedestal induction by enteropathogenic E. coli and promotes bacterial filamentation in vitro". PLOS ONE. 14 (3): e0213580. Bibcode:2019PLoSO..1413580M. doi:10.1371/journal.pone.0213580. PMC 6407759. PMID 30849110.
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