Filamentation

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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, also termed conditional 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] The cells that result from elongation without division have multiple chromosomal copies.[2] 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 protecting bacteria from protozoan predation and neutrophil phagocytosis by making ingestion of cells more difficult.[2][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 treated with various chemical and physical agents (e.g. DNA synthesis-inhibiting antibiotics, UV light).[3] Some of the key genes involved in filamentation in E. coli include sulA and minCD.[8]

Filament formation[edit]

Direct, extrinsic causes of filamentation[edit]

Filamentation can be induced by the inhibition of cell division via exposure to antibiotics that inhibit divisome assembly [9] or septal peptidoglycan synthesis.[10] 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] Bacteriophage infection can also result in filamentation via the expression of proteins that inhibit divisome assembly.[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]

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[edit]

Filamentation is often a consequence of environmental stress, or starvation, and has been observed in response to temperature shocks,[15] low water availability,[16] high osmolarity,[17] extreme pH,[18] and UV exposure.[19] UV light damages bacterial DNA and induces filamentation via the SOS response.[3][20]

Starvation-induced filamentation[edit]

Nutritional changes may also cause bacterial filamentation.[8] For example, if bacteria are deprived of the nucleobase thymine by starvation, this disrupts DNA synthesis and induces SOS-mediated filamentation.[3][21]

Nutrient-induced filamentation[edit]

Several macronutrients and biomolecules can cause bacterial cells to filament, including several amino acids: glutamine, proline and arginine and branched-chain amino acids.[22] 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.[23] Filamentation is also induced in nutrient-rich conditions by Bordetella atropi where the bacterial divisome is suppressed by the highly conserved UDP-glucose pathway, enabling bacteria to detect entry into host cells and transit into neighboring cells [24].

Intrinsic dysbiosis-induced filamentation[edit]

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). Other The overcrowding of the periplasm or envelope can also which can prevent normal divisome function, resulting in filamentation.[26]

Filamentation and biotic interactions[edit]

Several examples of filamentation that results from biotic interactions between organisms have been reported. Filamentous cells are resistant to ingestion by bacterivores and environmental conditions generated during predation can trigger filamentation.[27] Filamentation can also be induced by signalling factors produced by other bacteria.[28] Agrobacterium spp. filaments in proximity to plant roots (Finer et al., 2001) while E. coli filaments when exposed to plant extracts.[29]

See also[edit]

References[edit]

  1. ^ 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. PMID 34929753. S2CID 245412965.
  2. ^ a b 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.
  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.
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  19. ^ 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): 871–81. doi:10.1111/j.1751-1097.2010.00758.x. PMID 20528974. S2CID 45542973.
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  21. ^ 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.
  22. ^ Jensen, RH; Woolfolk, CA (August 1985). "Formation of Filaments by Pseudomonas putida". Applied and Environmental Microbiology. 50 (2): 364–72. Bibcode:1985ApEnM..50..364J. doi:10.1128/aem.50.2.364-372.1985. PMC 238629. PMID 16346856.
  23. ^ 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. PMID 34929753. S2CID 245412965.
  24. ^ Tran, TD; Ali, MA; Lee, D; Félix, MA; Luallen, RJ (4 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, Sanchari; Bershtein, Shimon; Adkar, Bharat V; Woodard, Jaie; Shakhnovich, Eugene I (2021-06-01). "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. ISSN 1744-4292. PMC 8236904. PMID 34180142.
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  29. ^ 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.