SpringerLink
Log in

Filamentous morphology of bacterial pathogens: regulatory factors and control strategies

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Several studies have demonstrated that when exposed to physical, chemical, and biological stresses in the environment, many bacteria (Gram-positive and Gram-negative) change their morphology from a normal cell to a filamentous shape. The formation of filamentous morphology is one of the survival strategies against environmental stress and protection against phagocytosis or protist predators. Numerous pathogenic bacteria have shown filamentous morphologies when examined in vivo or in vitro. During infection, certain pathogenic bacteria adopt a filamentous shape inside the cell to avoid phagocytosis by immune cells. Filamentous morphology has also been seen in biofilms formed on biotic or abiotic surfaces by certain bacteria. As a result, in addition to protecting against phagocytosis by immune cells or predators, the filamentous shape aids in biofilm adhesion or colonization to biotic or abiotic surfaces. Furthermore, these filamentous morphologies of bacterial pathogens lead to antimicrobial drug resistance. Clinically, filamentous morphology has become one of the most serious challenges in treating bacterial infection. The current review went into great detail about the various factors involved in the change of filamentous morphology and the underlying mechanisms. In addition, the review discussed a control strategy for suppressing filamentous morphology in order to combat bacterial infections. Understanding the mechanism underlying the filamentous morphology induced by various environmental conditions will aid in drug development and lessen the virulence of bacterial pathogens.

Key points

• The bacterial filamentation morphology is one of the survival mechanisms against several environmental stress conditions and protection from phagocytosis by host cells and protist predators.

• The filamentous morphologies in bacterial pathogens contribute to enhanced biofilm formation, which develops resistance properties against antimicrobial drugs.

• Filamentous morphology has become one of the major hurdles in treating bacterial infection, hence controlling strategies employed for inhibiting the filamentation morphology from combating bacterial infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abeysundara PDA, Dhowlaghar N, Nannapaneni R (2019) Influence of cold stress on the survival of Listeria monocytogenes Bug600 and ScottA in lethal alkali, acid and oxidative stress. LWT-Food Sci Technol 100:40–47

    Google Scholar 

  • Agarwal J, Srivastava S, Singh M (2012) Pathogenomics of uropathogenic Escherichia coli. Indian J Med Microbiol 30(2):141–149

    CAS  PubMed  Google Scholar 

  • Allison C, Coleman N, Jones PL, Hughes C (1992) Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect Immun 60(11):4740–4746. https://doi.org/10.1128/iai.60.11.4740-4746.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen TE, Khandige S, Madelung M, Brewer J, Kolmos HJ, Møller-Jensen J (2012) Escherichia coli uropathogenesis in vitro: invasion, cellular escape, and secondary infection analyzed in a human bladder cell infection model. Infect Immun 80(5):1858–1867

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andreu JM, Schaffner-Barbero C, Huecas S, Alonso D, Lopez-Rodriguez ML, Ruiz-Avila LB, Nunez-Ramirez R, Llorca O, Martin-Galiano AJ (2010) The antibacterial cell division inhibitor PC190723 is an FtsZ polymer-stabilizing agent that induces filament assembly and condensation. J Biol Chem 285(19):14239–14246. https://doi.org/10.1074/jbc.M109.094722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anutrakunchai C, Bolscher JG, Krom BP, Kanthawong S, Chareonsudjai S, Taweechaisupapong S (2018) Impact of nutritional stress on drug susceptibility and biofilm structures of Burkholderia pseudomallei and Burkholderia thailandensis grown in static and microfluidic systems. PLoS ONE 13(3):e0194946

    PubMed  PubMed Central  Google Scholar 

  • Araújo-Bazán L, Ruiz-Avila LB, Andreu D, Huecas S, Andreu JM (2016) Cytological profile of antibacterial FtsZ inhibitors and synthetic peptide MciZ. Front Microbiol 7:1558–1558. https://doi.org/10.3389/fmicb.2016.01558

    Article  PubMed  PubMed Central  Google Scholar 

  • Arena ET, Auweter SD, Antunes LCM, Vogl AW, Han J, Guttman JA, Croxen MA, Menendez A, Covey SD, Borchers CH (2011) The deubiquitinase activity of the Salmonella pathogenicity island 2 effector, SseL, prevents accumulation of cellular lipid droplets. Infect Immun 79(11):4392–4400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Argüelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174(4):217–224

    PubMed  Google Scholar 

  • Aromdee C, Sriubolmas N, Wiyakrutta S, Suebsasna S, Khunkitti W (2011) Effect of the derivatives of andrographolide on the morphology of Bacillus subtilis. Arch Pharm Res 34(1):71–77

    CAS  PubMed  Google Scholar 

  • Bartlett D (2002) Pressure effects on in vivo microbial processes. Biochim Biophys Acta 1595(1–2):367–381

    CAS  PubMed  Google Scholar 

  • Bellio P, Brisdelli F, Perilli M, Sabatini A, Bottoni C, Segatore B, Setacci D, Amicosante G, Celenza G (2014) Curcumin inhibits the SOS response induced by levofloxacin in Escherichia coli. Phytomedicine 21(4):430–434. https://doi.org/10.1016/j.phymed.2013.10.011

    Article  CAS  PubMed  Google Scholar 

  • Bellio P, Di Pietro L, Mancini A, Piovano M, Nicoletti M, Brisdelli F, Tondi D, Cendron L, Franceschini N, Amicosante G, Perilli M, Celenza G (2017) SOS response in bacteria: inhibitory activity of lichen secondary metabolites against Escherichia coli RecA protein. Phytomedicine 29:11–18. https://doi.org/10.1016/j.phymed.2017.04.001

    Article  CAS  PubMed  Google Scholar 

  • Bellio P, Mancini A, Di Pietro L, Cracchiolo S, Franceschini N, Reale S, de Angelis F, Perilli M, Amicosante G, Spyrakis F, Tondi D, Cendron L, Celenza G (2020) Inhibition of the transcriptional repressor LexA: withstanding drug resistance by inhibiting the bacterial mechanisms of adaptation to antimicrobials. Life Sci 241:117116. https://doi.org/10.1016/j.lfs.2019.117116

    Article  CAS  PubMed  Google Scholar 

  • Ben-Jacob E (2003) Bacterial self–organization: co–enhancement of complexification and adaptability in a dynamic environment. Philos Trans A Math Phys Eng Sci 361(1807):1283–1312

    PubMed  Google Scholar 

  • Bendezú FO, Hale CA, Bernhardt TG, de Boer PA (2009) RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. Embo J 28(3):193–204. https://doi.org/10.1038/emboj.2008.264

    Article  CAS  PubMed  Google Scholar 

  • Bereksi N, Gavini F, Bénézech T, Faille C (2002) Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. J Appl Microbiol 92(3):556–565. https://doi.org/10.1046/j.1365-2672.2002.01564.x

    Article  CAS  PubMed  Google Scholar 

  • Berlanga M, Viñas M, Guerrero R (2016) Bacterial predation: natural guns to control infection. New Weapons Control Bacterial Growth, Springer. Cham 489–508

  • Bessarab DA, Kaberdin VR, Wei C-L, Liou G-G, Lin-Chao S (1998) RNA components of Escherichia coli degradosome: evidence for rRNA decay. Proc Natl Acad Sci U S A 95(6):3157–3161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beuria TK, Santra MK, Panda D (2005) Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling. Biochemistry 44(50):16584–16593. https://doi.org/10.1021/bi050767+

    Article  CAS  PubMed  Google Scholar 

  • Bien J, Sokolova O, Bozko P (2012) Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol 2012:1–15

  • Bisson-Filho AW, Discola KF, Castellen P, Blasios V, Martins A, Sforça ML, Garcia W, Zeri ACM, Erickson HP, Dessen A (2015) FtsZ filament cap** by MciZ, a developmental regulator of bacterial division. Proc Natl Acad Sci U S A 112(17):E2130–E2138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bjarnsholt T (2013) The role of bacterial biofilms in chronic infections. APMIS 121:1–58

    Google Scholar 

  • Booth IR, Cash P, O’byrne C (2002) Sensing and adapting to acid stress. Antonie Van Leeuwenhoek 81(1):33–42

    CAS  Google Scholar 

  • Bos J, Zhang Q, Vyawahare S, Rogers E, Rosenberg SM, Austin RH (2015) Emergence of antibiotic resistance from multinucleated bacterial filaments. Proc Natl Acad Sci U S A 112(1):178–183. https://doi.org/10.1073/pnas.1420702111

    Article  CAS  PubMed  Google Scholar 

  • Brown HL, Reuter M, Salt LJ, Cross KL, Betts RP, van Vliet AHM (2014) Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl Environ Microbiol 80(22):7053–7060. https://doi.org/10.1128/AEM.02614-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brudzynski K, Sjaarda C (2014) Antibacterial compounds of Canadian honeys target bacterial cell wall inducing phenotype changes, growth inhibition and cell lysis that resemble action of β-lactam antibiotics. PLoS ONE 9(9):e106967. https://doi.org/10.1371/journal.pone.0106967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buijs J, Dofferhoff AM, Mouton J, Wagenvoort J, Van Der Meer J (2008) Concentration-dependency of β-lactam-induced filament formation in Gram-negative bacteria. Clin Microbiol Infect 14(4):344–349

    CAS  PubMed  Google Scholar 

  • Burby PE, Simmons LA (2020) Regulation of cell division in bacteria by monitoring genome integrity and DNA replication status. J Bacteriol 202(2):e00408-e419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bush K, Bradford PA (2016) β-Lactams and β-lactamase inhibitors: an overview. Cold Spring Harb Perspect Med 6(8):a025247. https://doi.org/10.1101/cshperspect.a025247

  • Cabre EJ, Monterroso B, Alfonso C, Sanchez-Gorostiaga A, Reija B, Jimenez M, Vicente M, Zorrilla S, Rivas G (2015) The nucleoid occlusion SlmA protein accelerates the disassembly of the FtsZ protein polymers without affecting their GTPase activity. PLoS ONE 10(5):e0126434

    PubMed  PubMed Central  Google Scholar 

  • Cameron A, Frirdich E, Huynh S, Parker CT, Gaynor EC (2012) Hyperosmotic stress response of Campylobacter jejuni. J Bacteriol 194(22):6116–6130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cayley S, Record MT (2003) Roles of cytoplasmic osmolytes, water, and crowding in the response of Escherichia coli to osmotic stress: biophysical basis of osmoprotection by glycine betaine. Biochemistry 42(43):12596–12609

    CAS  PubMed  Google Scholar 

  • Cayron J, Dedieu A, Lesterlin C (2020) Bacterial filament division dynamics allows rapid post-stress cell proliferation. BioRxiv. https://doi.org/10.1101/2020.03.16.993345

  • Chauhan A, Madiraju MV, Fol M, Lofton H, Maloney E, Reynolds R, Rajagopalan M (2006) Mycobacterium tuberculosis cells growing in macrophages are filamentous and deficient in FtsZ rings. J Bacteriol 188(5):1856–1865

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen K, Sun GW, Chua KL, Gan Y-H (2005) Modified virulence of antibiotic-induced Burkholderia pseudomallei filaments. Antimicrob Agents Chemother 49(3):1002–1009

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chung H, Bang W, Drake M (2006) Stress response of Escherichia coli. Compr Rev Food Sci Food Saf 5(3):52–64

    CAS  Google Scholar 

  • Ciofu O, Moser C, Jensen PØ, Høiby N (2022) Tolerance and resistance of microbial biofilms. Nat Rev Microbiol 1–15. https://doi.org/10.1038/s41579-022-00682-4

  • Dasgupta D (2009) Novel compound with potential of an antibacterial drug targets FtsZ protein. Biochem J 423(1):e1–e3. https://doi.org/10.1042/bj20091226

    Article  CAS  PubMed  Google Scholar 

  • Davis KJ, Vogel P, Fritz DL, Steele KE (1997) Bacterial filamentation of Yersinia pestis by beta-lactam antibiotics in experimentally infected mice. Arch Pathol Lab Med 121(8):865

    CAS  PubMed  Google Scholar 

  • de Boer PA, Crossley RE, Rothfield LI (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56(4):641–9. https://doi.org/10.1016/0092-8674(89)90586-2

    Article  PubMed  Google Scholar 

  • de Boer PA, Crossley RE, Rothfield LI (1990) Central role for the Escherichia coli minC gene product in two different cell division-inhibition systems. Proc Natl Acad Sci U S A 87(3):1129–1133. https://doi.org/10.1073/pnas.87.3.1129

    Article  PubMed  PubMed Central  Google Scholar 

  • de Boer PA, Crossley RE, Rothfield LI (1992) Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol 174(1):63–70. https://doi.org/10.1128/jb.174.1.63-70.1992

    Article  PubMed  PubMed Central  Google Scholar 

  • de León L, Beltrán B, Moujir L (2005) Antimicrobial activity of 6-oxophenolic triterpenoids. Mode of action against Bacillus subtilis. Planta Med 71(04):313–319

    PubMed  Google Scholar 

  • Dean CR, Barkan DT, Bermingham A, Blais J, Casey F, Casarez A, Colvin R, Fuller J, Jones AK, Li C (2018) Mode of action of the monobactam LYS228 and mechanisms decreasing in vitro susceptibility in Escherichia coli and Klebsiella pneumoniae. Antimicrob Agents Chemother 62(10):e01200-e1218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Den Besten HM, Mols M, Moezelaar R, Zwietering MH, Abee T (2009) Phenotypic and transcriptomic analyses of mildly and severely salt-stressed Bacillus cereus ATCC 14579 cells. Appl Environ Microbiol 75(12):4111–4119

    Google Scholar 

  • Dev Kumar G, Macarisin D, Micallef Shirley A, Schaffner Donald W (2019) Salmonella enterica filamentation induced by pelargonic acid is a transient morphotype. Appl Environ Microbiol 85(2):e02191-e2218. https://doi.org/10.1128/AEM.02191-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Dofferhoff A, Esselink M, de Vries-Hospers H, Av Z, Bom V, Weits J, Vellenga E (1993) The release of endotoxin from antibiotic-treated Escherichia coli and the production of tumour necrosis factor by human monocytes. J Antimicrob Chemother 31(3):373–384

    CAS  PubMed  Google Scholar 

  • Domadia P, Swarup S, Bhunia A, Sivaraman J, Dasgupta D (2007) Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde. Biochem Pharmacol 74(6):831–840

    CAS  PubMed  Google Scholar 

  • Elhadi D, Lv L, Jiang X-R, Wu H, Chen G-Q (2016) CRISPRi engineering E. coli for morphology diversification. Metab Eng 38:358–369

    CAS  PubMed  Google Scholar 

  • Elsen NL, Lu J, Parthasarathy G, Reid JC, Sharma S, Soisson SM, Lumb KJ (2012) Mechanism of action of the cell-division inhibitor PC190723: modulation of FtsZ assembly cooperativity. J Am Chem Soc 134(30):12342–12345. https://doi.org/10.1021/ja303564a

    Article  CAS  PubMed  Google Scholar 

  • England K, Crew R, Slayden RA (2011) Mycobacterium tuberculosis septum site determining protein, Ssd encoded by rv3660c, promotes filamentation and elicits an alternative metabolic and dormancy stress response. BMC Microbiol 11(1):1–12

    Google Scholar 

  • Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47(1):103–118. https://doi.org/10.1046/j.1365-2958.2003.03313.x

    Article  CAS  PubMed  Google Scholar 

  • Fang FC, Frawley ER, Tapscott T, Vázquez-Torres A (2016) Bacterial stress responses during host infection. Cell Host Microbe 20(2):133–43. https://doi.org/10.1016/j.chom.2016.07.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filiatrault MJ, Picardo KF, Ngai H, Passador L, Iglewski BH (2006) Identification of Pseudomonas aeruginosa genes involved in virulence and anaerobic growth. Infect Immun 74(7):4237–4245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flannigan KL, Denning TL (2018) Segmented filamentous bacteria-induced immune responses: a balancing act between host protection and autoimmunity. Immunology 154(4):537–546

    CAS  PubMed Central  Google Scholar 

  • Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13(5):269–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fredborg M, Rosenvinge FS, Spillum E, Kroghsbo S, Wang M, Sondergaard TE (2015) Automated image analysis for quantification of filamentous bacteria. BMC Microbiol 15(1):1–8

    Google Scholar 

  • Fuchino K, Flärdh K, Dyson P, Ausmees N (2016) Cell-biological studies of osmotic shock response in Streptomyces spp. J Bacteriol 199(1):e00465-e516. https://doi.org/10.1128/JB.00465-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garrett TR, Bhakoo M, Zhang Z (2008) Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18(9):1049–1056

    CAS  Google Scholar 

  • Ghaffar NM, Connerton PL, Connerton IF (2015) Filamentation of Campylobacter in broth cultures. Front Microbiol 6:657

    PubMed  PubMed Central  Google Scholar 

  • Gilbert P, Maira-Litran T, McBain AJ, Rickard AH, Whyte FW (2002) The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol 46:202–256

    PubMed  Google Scholar 

  • Giotis ES, Blair IS, McDowell DA (2007) Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress. Int J Food Microbiol 120(3):250–258. https://doi.org/10.1016/j.ijfoodmicro.2007.08.036

    Article  CAS  PubMed  Google Scholar 

  • Godden S, Bey R, Lorch K, Farnsworth R, Rapnicki P (2008) Ability of organic and inorganic bedding materials to promote growth of environmental bacteria. J Dairy Sci 91(1):151–159

    CAS  PubMed  Google Scholar 

  • Haeusser DP, Hoashi M, Weaver A, Brown N, Pan J, Sawitzke JA, Thomason LC, Court DL, Margolin W (2014) The kil peptide of bacteriophage λ blocks Escherichia coli cytokinesis via ZipA-dependent inhibition of FtsZ assembly. PLOS Genet 10(3):e1004217. https://doi.org/10.1371/journal.pgen.1004217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris LK, Theriot JA (2016) Relative rates of surface and volume synthesis set bacterial cell size. Cell 165(6):1479–1492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harshey RM, Matsuyama T (1994) Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci U S A 91(18):8631–8635. https://doi.org/10.1073/pnas.91.18.8631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinrich K, Leslie DJ, Morlock M, Bertilsson S, Jonas K (2019) Molecular basis and ecological relevance of Caulobacter cell filamentation in freshwater habitats. Mbio 10(4):e01557-e1619

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heinrich K, Sobetzko P, Jonas K (2016) A kinase-phosphatase switch transduces environmental information into a bacterial cell cycle circuit. PLOS Genet 12(12):e1006522. https://doi.org/10.1371/journal.pgen.1006522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoeniger JF (1966) Cellular changes accompanying the swarming of Proteus mirabilis. II. Observations of stained organisms. Can J Microbiol 12(1):113–23. https://doi.org/10.1139/m66-017

    Article  CAS  PubMed  Google Scholar 

  • Horvath DJ, Li B, Casper T, Partida-Sanchez S, Hunstad DA, Hultgren SJ, Justice SS (2011) Morphological plasticity promotes resistance to phagocyte killing of uropathogenic Escherichia coli. Microbes Infect 13(5):426–437. https://doi.org/10.1016/j.micinf.2010.12.004

    Article  CAS  PubMed  Google Scholar 

  • Hou S, Jia Z, Kryszczuk K, Chen D, Wang L, Holyst R, Feng X (2020) Joint effect of surfactants and cephalexin on the formation of Escherichia coli filament. Ecotox Environ Safe 199:110750

    CAS  Google Scholar 

  • Huisman O, D’Ari R (1981) An inducible DNA replication–cell division coupling mechanism in E. coli. Nature 290(5809):797–799. https://doi.org/10.1038/290797a0

    Article  CAS  PubMed  Google Scholar 

  • Huisman O, D’Ari R, Gottesman S (1984) Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc Natl Acad Sci U S A 81(14):4490–4494. https://doi.org/10.1073/pnas.81.14.4490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humphrey S, MacVicar T, Stevenson A, Roberts M, Humphrey TJ, Jepson MA (2011) SulA-induced filamentation in Salmonella enterica serovar Typhimurium: effects on SPI-1 expression and epithelial infection. J Appl Microbiol 111(1):185–196. https://doi.org/10.1111/j.1365-2672.2011.05022.x

    Article  CAS  PubMed  Google Scholar 

  • Ingham CJ, van den Ende M, Wever PC, Schneeberger PM (2006) Rapid antibiotic sensitivity testing and trimethoprim-mediated filamentation of clinical isolates of the Enterobacteriaceae assayed on a novel porous culture support. J Med Microbiol 55(11):1511–1519

    CAS  PubMed  Google Scholar 

  • Iosifidis G, Duggin IG (2020) Distinct morphological fates of uropathogenic Escherichia coli intracellular bacterial communities: dependency on urine composition and pH. Infect Immun 88(9):e00884-e919

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jaiswal R, Beuria TK, Mohan R, Mahajan SK, Panda D (2007) Totarol inhibits bacterial cytokinesis by perturbing the assembly dynamics of FtsZ. Biochemistry 46(14):4211–4220. https://doi.org/10.1021/bi602573e

    Article  CAS  PubMed  Google Scholar 

  • ** Y, Zheng H, Ibanez ACS, Patil PD, Lv S, Luo M, Duncan TM, Luk YY (2020) Cell-wall-targeting antibiotics cause lag-phase bacteria to form surface-mediated filaments promoting the formation of biofilms and aggregates. ChemBioChem 21(6):825–835

    CAS  PubMed  Google Scholar 

  • Johnson JE, Lackner LL, de Boer PA (2002) Targeting of (D)MinC/MinD and (D)MinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ rings. J Bacteriol 184(11):2951–2962. https://doi.org/10.1128/jb.184.11.2951-2962.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones TH, Vail KM, McMullen LM (2013) Filament formation by foodborne bacteria under sublethal stress. Int J Food Microbiol 165(2):97–110

    CAS  PubMed  Google Scholar 

  • Jørgensen F, Stephens PJ, Knøchel S (1995) The effect of osmotic shock and subsequent adaptation on the thermotolerance and cell morphology of Listeria monocytogenes. J Appl Bacteriol 79(3):274–281. https://doi.org/10.1111/j.1365-2672.1995.tb03137.x

    Article  Google Scholar 

  • Justice SS, Harrison A, Becknell B, Mason KM (2014) Bacterial differentiation, development, and disease: mechanisms for survival. FEMS Microbiol Lett 360(1):1–8

    CAS  PubMed  Google Scholar 

  • Justice SS, Hunstad DA, Cegelski L, Hultgren SJ (2008) Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 6(2):162–168

    CAS  PubMed  Google Scholar 

  • Justice SS, Hunstad DA, Seed PC, Hultgren SJ (2006) Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc Natl Acad Sci USA 103(52):19884–19889. https://doi.org/10.1073/pnas.0606329104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaale LD, Eikevik TM, Rustad T, Kolsaker K (2011) Superchilling of food: a review. J Food Eng 107(2):141–146

    Google Scholar 

  • Kalmokoff M, Lanthier P, Tremblay T-L, Foss M, Lau PC, Sanders G, Austin J, Kelly J, Szymanski CM (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188(12):4312–4320. https://doi.org/10.1128/jb.01975-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karasz DC, Weaver AI, Buckley DH, Wilhelm RC (2022) Conditional filamentation as an adaptive trait of bacteria and its ecological significance in soils. Environ Microbiol 24(1):1–17

    CAS  PubMed  Google Scholar 

  • Kawarai T, Wachi M, Ogino H, Furukawa S, Suzuki K, Ogihara H, Yamasaki M (2004) SulA-independent filamentation of Escherichia coli during growth after release from high hydrostatic pressure treatment. Appl Microbiol Biotechnol 64(2):255–262

    CAS  PubMed  Google Scholar 

  • Khan F, Jeong M-C, Park S-K, Kim S-K, Kim Y-M (2019) Contribution of chitooligosaccharides to biofilm formation, antibiotics resistance and disinfectants tolerance of Listeria monocytogenes. Microb Pathog 136:103673. https://doi.org/10.1016/j.micpath.2019.103673

    Article  CAS  PubMed  Google Scholar 

  • Khan F, Lee J-W, Javaid A, Park S-K, Kim Y-M (2020) Inhibition of biofilm and virulence properties of Pseudomonas aeruginosa by sub-inhibitory concentrations of aminoglycosides. Microb Pathog 146:104249. https://doi.org/10.1016/j.micpath.2020.104249

    Article  CAS  PubMed  Google Scholar 

  • Khan F, Yu H, Kim Y-M (2020) Bactericidal activity of usnic acid-chitosan nanoparticles against persister cells of biofilm-forming pathogenic bacteria. Mar Drugs 18(5):270. https://doi.org/10.3390/md18050270

    Article  CAS  PubMed Central  Google Scholar 

  • Khandige S, Asferg CA, Rasmussen KJ, Larsen MJ, Overgaard M, Andersen TE, Møller-Jensen J (2016) DamX controls reversible cell morphology switching in uropathogenic Escherichia coli. Mbio 7(4):e00642-e716

    PubMed  PubMed Central  Google Scholar 

  • Kim WR, Aung MM, Chang YS, Makatsoris C (2015) Freshness Gauge based cold storage management: a method for adjusting temperature and humidity levels for food quality. Food Control 47:510–519

    Google Scholar 

  • Kiro R, Molshanski-Mor S, Yosef I, Milam SL, Erickson HP, Qimron U (2013) Gene product 0.4 increases bacteriophage T7 competitiveness by inhibiting host cell division. Proc Natl Acad Sci U.S.A. 110(48):19549–19554. https://doi.org/10.1073/pnas.1314096110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreuzer KN (2013) DNA damage responses in prokaryotes: regulating gene expression, modulating growth patterns, and manipulating replication forks. Cold Spring Harb Perspect Biol 5(11):a012674

    PubMed  PubMed Central  Google Scholar 

  • Kusuma KD, Payne M, Ung AT, Bottomley AL, Harry EJ (2019) FtsZ as an antibacterial target: status and guidelines for progressing this avenue. ACS Infect Dis 5(8):1279–1294

    CAS  PubMed  Google Scholar 

  • Lau SY, Zgurskaya HI (2005) Cell division defects in Escherichia coli deficient in the multidrug efflux transporter AcrEF-TolC. J Bacteriol 187(22):7815–7825. https://doi.org/10.1128/jb.187.22.7815-7825.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee B-H, Hébraud M, Bernardi T (2017) Increased adhesion of Listeria monocytogenes strains to abiotic surfaces under cold stress. Front Microbiol 8:2221

    PubMed  PubMed Central  Google Scholar 

  • Lee H, Lee DG (2019) Arenicin-1-induced apoptosis-like response requires RecA activation and hydrogen peroxide against Escherichia coli. Curr Genet 65(1):167–177

    CAS  PubMed  Google Scholar 

  • Lee W, Lee DG (2014) Lycopene-induced hydroxyl radical causes oxidative DNA damage in Escherichia coli. J Microbiol Biotechnol 24(9):1232–1237

    CAS  PubMed  Google Scholar 

  • Leistner L (2000) Basic aspects of food preservation by hurdle technology. Int J Food Microbiol 55(1–3):181–186

    CAS  PubMed  Google Scholar 

  • Leroy M, Cabral H, Figueira M, Bouchet V, Huot H, Ram S, Pelton SI, Goldstein R (2007) Multiple consecutive lavage samplings reveal greater burden of disease and provide direct access to the nontypeable Haemophilus influenzae biofilm in experimental otitis media. Infect Immun 75(8):4158–4172. https://doi.org/10.1128/iai.00318-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewin C, Amyes S (1991) The role of the SOS response in bacteria exposed to zidovudine or trimethoprim. J Med Microbiol 34(6):329–332

    CAS  PubMed  Google Scholar 

  • Liou G-G, Chang H-Y, Lin C-S, Lin-Chao S (2002) DEAD box RhlB RNA helicase physically associates with exoribonuclease PNPase to degrade double-stranded RNA independent of the degradosome-assembling region of RNase E. J Biol Chem 277(43):41157–41162

    CAS  PubMed  Google Scholar 

  • Liu MM, Coleman S, Wilkinson L, Smith ML, Hoang T, Niyah N, Mukherjee M, Huynh S, Parker CT, Kovac J, Hancock REW, Gaynor EC (2020) Unique inducible filamentous motility identified in pathogenic Bacillus cereus group species. ISME J 14(12):2997–3010. https://doi.org/10.1038/s41396-020-0728-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loewen PC, Hengge-Aronis R (1994) The role of the sigma factor σS (KatF) in bacterial global regulation. Annu Rev Microbiol 48(1):53–80

    CAS  PubMed  Google Scholar 

  • Lushchak V (2001) Oxidative stress and mechanisms of protection against it in bacteria. Biochem Mosc 66(5):476–489

    CAS  Google Scholar 

  • Lv L, Ren Y-L, Chen J-C, Wu Q, Chen G-Q (2015) Application of CRISPRi for prokaryotic metabolic engineering involving multiple genes, a case study: controllable P (3HB-co-4HB) biosynthesis. Metab Eng 29:160–168

    CAS  PubMed  Google Scholar 

  • Maguin E, Lutkenhaus J, D’ari R (1986) Reversibility of SOS-associated division inhibition in Escherichia coli. J Bacteriol 166(3):733–738

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mañas P, Mackey BM (2004) Morphological and physiological changes induced by high hydrostatic pressure in exponential-and stationary-phase cells of Escherichia coli: relationship with cell death. Appl Environ Microbiol 70(3):1545–1554

    PubMed  PubMed Central  Google Scholar 

  • Marathe SA, Kumar R, Ajitkumar P, Nagaraja V, Chakravortty D (2013) Curcumin reduces the antimicrobial activity of ciprofloxacin against Salmonella Typhimurium and Salmonella typhi. J Antimicrob Chemother 68(1):139–152

    CAS  PubMed  Google Scholar 

  • Masuda H, Tan Q, Awano N, Wu KP, Inouye M (2012) YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol Microbiol 84(5):979–989

    CAS  PubMed  Google Scholar 

  • Mateos-Gil P, Tarazona P, Vélez M (2019) Bacterial cell division: modeling FtsZ assembly and force generation from single filament experimental data. FEMS Microbiol Rev 43(1):73–87

    CAS  PubMed  Google Scholar 

  • Mattick KL, Phillips LE, Jørgensen F, Lappin-Scott HM, Humphrey TJ (2003) Filament formation by Salmonella spp. inoculated into liquid food matrices at refrigeration temperatures, and growth patterns when warmed. J Food Prot 66(2):215–9. https://doi.org/10.4315/0362-028x-66.2.215

    Article  PubMed  Google Scholar 

  • Mattick KL, Rowbury RJ, Humphrey TJ (2003b ) Morphological changes to Escherichia coli O157: H7, commensal E. coli and Salmonella spp in response to marginal growth conditions, with special reference to mildly stressing temperatures. Sci Prog (1933- ) 86(1/2):103–113

  • McLaughlin HP, Bugrysheva J, Sue D (2020) Optical microscopy reveals the dynamic nature of B. pseudomallei morphology during β-lactam antimicrobial susceptibility testing. BMC Microbiol 20(1):1-15

  • Miyoshi A, Rochat T, Gratadoux J-J, Le Loir Y, Oliveira SC, Langella P, Azevedo V (2003) Oxidative stress in Lactococcus lactis. Genet Mol Res 2(4):348–359

    CAS  PubMed  Google Scholar 

  • Mo CY, Culyba MJ, Selwood T, Kubiak JM, Hostetler ZM, Jurewicz AJ, Keller PM, Pope AJ, Quinn A, Schneck J, Widdowson KL, Kohli RM (2018) Inhibitors of LexA autoproteolysis and the bacterial SOS response discovered by an academic-industry partnership. ACS Infect Dis 4(3):349–359. https://doi.org/10.1021/acsinfecdis.7b00122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modenutti B, Balseiro E, Corno G, Callieri C, Bertoni R, Caravati E (2010) Ultraviolet radiation induces filamentation in bacterial assemblages from North Andean Patagonian Lakes. Photochem Photobiol 86(4):871–881. https://doi.org/10.1111/j.1751-1097.2010.00758.x

    Article  CAS  PubMed  Google Scholar 

  • Möller J, Emge P, Vizcarra IA, Kollmannsberger P, Vogel V (2013) Bacterial filamentation accelerates colonization of adhesive spots embedded in biopassive surfaces. New J Phys 15(12):125016. https://doi.org/10.1088/1367-2630/15/12/125016

    Article  CAS  Google Scholar 

  • Monterroso B, Zorrilla S, Sobrinos-Sanguino M, Robles-Ramos MA, López-Álvarez M, Margolin W, Keating CD, Rivas G (2019) Bacterial FtsZ protein forms phase-separated condensates with its nucleoid-associated inhibitor SlmA. EMBO Rep 20(1):e45946

    PubMed  Google Scholar 

  • Mückl A, Schwarz-Schilling M, Fischer K, Simmel FC (2018) Filamentation and restoration of normal growth in Escherichia coli using a combined CRISPRi sgRNA/antisense RNA approach. PLoS ONE 13(9):e0198058

    PubMed  PubMed Central  Google Scholar 

  • Muraleedharan S, Freitas C, Mann P, Glatter T, Ringgaard S (2018) A cell length-dependent transition in MinD-dynamics promotes a switch in division-site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells. Mol Microbiol 109(3):365–384. https://doi.org/10.1111/mmi.13996

    Article  CAS  PubMed  Google Scholar 

  • Murashko ON, Lin-Chao S (2017) Escherichia coli responds to environmental changes using enolasic degradosomes and stabilized DicF sRNA to alter cellular morphology. Proc Natl Acad Sci USA 114(38):E8025–E8034. https://doi.org/10.1073/pnas.1703731114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navarro Llorens JM, Tormo A, Martínez-García E (2010) Stationary phase in gram-negative bacteria. FEMS MIcrobiol Rev 34(4):476–495

    PubMed  Google Scholar 

  • Ohashi Y, Chijiiwa Y, Suzuki K, Takahashi K, Nanamiya H, Sato T, Hosoya Y, Ochi K, Kawamura F (1999) The lethal effect of a benzamide derivative, 3-methoxybenzamide, can be suppressed by mutations within a cell division gene, Bacillus subtilis. J Bacteriol 181(4):1348–1351. https://doi.org/10.1128/JB.181.4.1348-1351.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ojha D, Patil KN (2019) p-Coumaric acid inhibits the Listeria monocytogenes RecA protein functions and SOS response: an antimicrobial target. Biochem Biophys Res Commun 517(4):655–661. https://doi.org/10.1016/j.bbrc.2019.07.093

    Article  CAS  PubMed  Google Scholar 

  • Ojkic N, Banerjee S (2021) Bacterial cell shape control by nutrient-dependent synthesis of cell division inhibitors. Biophys J 120(11):2079–2084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ, Chrétien F, Heitman J, Dromer F, Nielsen K (2010) Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 6(6):e1000953

    PubMed  PubMed Central  Google Scholar 

  • Okshevsky M, Meyer RL (2015) The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol 41(3):341–352

    CAS  PubMed  Google Scholar 

  • Painter RE, Adam GC, Arocho M, DiNunzio E, Donald RG, Dorso K, Genilloud O, Gill C, Goetz M, Hairston NN (2015) Elucidation of DnaE as the antibacterial target of the natural product, nargenicin. Chem Biol 22(10):1362–1373

    CAS  PubMed  Google Scholar 

  • Palmer KL, Brown SA, Whiteley M (2007) Membrane-bound nitrate reductase is required for anaerobic growth in cystic fibrosis sputum. J Bacteriol 189(12):4449–4455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Q, Zhou S, Yao F, Hou B, Huang Y, Hua D, Zheng Y, Qian Y (2011) Baicalein suppresses the SOS response system of Staphylococcus aureus induced by ciprofloxacin. Cell Physiol Biochem 28(5):1045–1050

    CAS  PubMed  Google Scholar 

  • Periti P, Mazzei T (1999) New criteria for selecting the proper antimicrobial chemotherapy for severe sepsis and septic shock. Int J Antimicrob Agents 12(2):97–105

    CAS  PubMed  Google Scholar 

  • Persat A, Nadell CD, Kim MK, Ingremeau F, Siryaporn A, Drescher K, Wingreen NS, Bassler BL, Gitai Z, Stone HA (2015) The mechanical world of bacteria. Cell 161(5):988–997

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petrovska I, Nüske E, Munder MC, Kulasegaran G, Malinovska L, Kroschwald S, Richter D, Fahmy K, Gibson K, Verbavatz J-M (2014) Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation. Elife 3:e02409

    PubMed Central  Google Scholar 

  • Phillips LE, Humphrey TJ, Lappin-Scott HM (1998) Chilling invokes different morphologies in two Salmonella enteritidis PT4 strains. J Appl Microbiol 84(5):820–826. https://doi.org/10.1046/j.1365-2672.1998.00417.x

    Article  CAS  PubMed  Google Scholar 

  • Piddock LJ, Wise R (1987) Induction of the SOS response in Escherichia coli by 4-quinolone antimicrobial agents. FEMS Microbiol Lett 41(3):289–294

    CAS  Google Scholar 

  • Pine L, Boone CJ (1967) Comparative cell wall analyses of morphological forms within the genus Actinomyces. J Bacteriol 94(4):875–883. https://doi.org/10.1128/jb.94.4.875-883.1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinzon NM, Cook AG, Ju LK (2013) Continuous rhamnolipid production using denitrifying Pseudomonas aeruginosa cells in hollow-fiber bioreactor. Biotechnol Prog 29(2):352–358

    CAS  PubMed  Google Scholar 

  • Plá CL, Cobos-Porras L (2015) Salinity: physiological impacts on legume nitrogen fixation Legume nitrogen fixation in a changing environment. Springer, pp 35–65

  • Poole K (2012) Bacterial stress responses as determinants of antimicrobial resistance. J Antimicrob Chemother 67(9):2069–2089. https://doi.org/10.1093/jac/dks196

    Article  CAS  PubMed  Google Scholar 

  • Popham DL, Young KD (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6(6):594–599

    CAS  PubMed  Google Scholar 

  • Portenier I, Waltimo T, Ørstavik D, Haapasalo M (2005) The susceptibility of starved, stationary phase, and growing cells of Enterococcus faecalis to endodontic medicaments. J Endod 31(5):380–386

    PubMed  Google Scholar 

  • Prabhakaran P, Ashraf MA, Aqma WS (2016) Microbial stress response to heavy metals in the environment. RSC Adv 6(111):109862–109877

    CAS  Google Scholar 

  • Prashar A, Bhatia S, Gigliozzi D, Martin T, Duncan C, Guyard C, Terebiznik MR (2013) Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages. J Cell Biol 203(6):1081–1097. https://doi.org/10.1083/jcb.201304095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pratt Zachary L, Chen B, Czuprynski Charles J, Wong Amy CL, Kaspar Charles W (2012) Characterization of osmotically induced filaments of Salmonella enterica. Appl Environ Microbiol 78(18):6704–6713. https://doi.org/10.1128/AEM.01784-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152(5):1173–1183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rai D, Singh JK, Roy N, Panda D (2008) Curcumin inhibits FtsZ assembly: an attractive mechanism for its antibacterial activity. Biochem J 410(1):147–155

    CAS  PubMed  Google Scholar 

  • Rangarajan AA, Koropatkin NM, Biteen JS (2020) Nutrient-dependent morphological variability of Bacteroides thetaiotaomicron. Microbiology 166(7):624–628

    CAS  PubMed  Google Scholar 

  • Rastogi RP, Kumar A, Tyagi MB, Sinha RP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic acids 2010:592980

  • Ratti RP, Gomes BC, Martinez RCR, Souza VM, Martinis ECPD (2010) Elongated cells of Listeria monocytogenes in biofilms in the presence of sucrose and bacteriocin-producing Leuconostoc mesenteroides A11. Food Sci Technol 30:1011–1016

    Google Scholar 

  • Rhee SJ, Lee JE, Lee CH (2011) Importance of lactic acid bacteria in Asian fermented foods. Microb Cell Fact 10:1–13

  • Rizzo MG, De Plano LM, Franco D (2020) Regulation of filamentation by bacteria and its impact on the productivity of compounds in biotechnological processes. Appl Microbiol Biotechnol 104(11):4631–4642. https://doi.org/10.1007/s00253-020-10590-3

    Article  CAS  PubMed  Google Scholar 

  • Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ (2007) Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 4(12):e329. https://doi.org/10.1371/journal.pmed.0040329

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosen DA, Pinkner JS, Jones JM, Walker JN, Clegg S, Hultgren SJ (2008) Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of FimK on type 1 pilus expression. Infect Immun 76(7):3337–3345

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenberger CM, Finlay BB (2002) Macrophages inhibit Salmonella typhimurium replication through MEK/ERK kinase and phagocyte NADPH oxidase activities. J Biol Chem 277(21):18753–18762. https://doi.org/10.1074/jbc.M110649200

    Article  CAS  PubMed  Google Scholar 

  • Rossetti V, Ammann TW, Thurnheer T, Bagheri HC, Belibasakis GN (2013) Phenotypic diversity of multicellular filamentation in oral streptococci. PLoS ONE 8(9):e76221

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rowbury RJ (2003) Temperature effects on biological systems: introduction. Sci Prog 86(1–2):1–8

    PubMed  Google Scholar 

  • Russell JB, Wilson DB (1996) Why are ruminal cellulolytic bacteria unable to digest cellulose at low pH? J Dairy Sci 79(8):1503–1509

    CAS  PubMed  Google Scholar 

  • Russell N (1990) Cold adaptation of microorganisms. P Philos Trans R Soc Lond B Biol Sci 326(1237):595–611

    CAS  Google Scholar 

  • Sarjit A, Ravensdale JT, Coorey R, Fegan N, Dykes GA (2019) Salmonella response to physical interventions employed in red meat processing facilities. Food Control 103:91–102

    CAS  Google Scholar 

  • Sarkar P, Yarlagadda V, Ghosh C, Haldar J (2017) A review on cell wall synthesis inhibitors with an emphasis on glycopeptide antibiotics. Medchemcomm 8(3):516–533

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schultenkämper K, Brito LF, Wendisch VF (2020) Impact of CRISPR interference on strain development in biotechnology. Biotechnol Appl Biochem 67(1):7–21

    PubMed  Google Scholar 

  • Sellars MJ, Hall SJ, Kelly DJ (2002) Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol 184(15):4187–4196. https://doi.org/10.1128/jb.184.15.4187-4196.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selwood T, Larsen BJ, Mo CY, Culyba MJ, Hostetler ZM, Kohli RM, Reitz AB, Baugh SDP (2018) Advancement of the 5-amino-1-(carbamoylmethyl)-1H-1,2,3-triazole-4-carboxamide scaffold to disarm the bacterial SOS response. Front Microbiol 9:2961. https://doi.org/10.3389/fmicb.2018.02961

    Article  PubMed  PubMed Central  Google Scholar 

  • Serbanescu D, Ojkic N, Banerjee S (2020) Nutrient-dependent trade-offs between ribosomes and division protein synthesis control bacterial cell size and growth. Cell Rep 32(12):108183

    CAS  PubMed  Google Scholar 

  • Serment-Guerrero J, Dominguez-Monroy V, Davila-Becerril J, Morales-Avila E, Fuentes-Lorenzo JL (2020) Induction of the SOS response of Escherichia coli in repair-defective strains by several genotoxic agents. Mutat Res Genet Toxicol Environ Mutagen 854:503196

    PubMed  Google Scholar 

  • Shi Z, Zou J, Zhang Z, Zhao X, Noriega J, Zhang B, Zhao C, Ingle H, Bittinger K, Mattei LM (2019) Segmented filamentous bacteria prevent and cure rotavirus infection. Cell 179(3):644–658.e13

  • Shiomi D, Sakai M, Niki H (2008) Determination of bacterial rod shape by a novel cytoskeletal membrane protein. Embo J 27(23):3081–3091. https://doi.org/10.1038/emboj.2008.234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiomi D, Toyoda A, Aizu T, Ejima F, Fujiyama A, Shini T, Kohara Y, Niki H (2013) Mutations in cell elongation genes mreB, mrdA and mrdB suppress the shape defect of RodZ-deficient cells. Mol Microbiol 87(5):1029–1044

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silva VO, Soares LO, Silva Júnior A, Mantovani HC, Chang Y-F, Moreira MAS (2014) Biofilm formation on biotic and abiotic surfaces in the presence of antimicrobials by Escherichia coli isolates from cases of bovine mastitis. Appl Environ Microbiol 80(19):6136–6145

    PubMed  PubMed Central  Google Scholar 

  • Silver LL (2006) Does the cell wall of bacteria remain a viable source of targets for novel antibiotics? Biochem Pharmacol 71(7):996–1005

    CAS  PubMed  Google Scholar 

  • Singh D, Majumdar AG, Gamre S, Subramanian M (2021) Membrane damage precedes DNA damage in hydroxychavicol treated E. coli cells and facilitates cooperativity with hydrophobic antibiotics. Biochimie 180:158–168. https://doi.org/10.1016/j.biochi.2020.11.008

    Article  CAS  PubMed  Google Scholar 

  • Smeulders MJ, Keer J, Speight RA, Williams HD (1999) Adaptation of Mycobacterium smegmatis to stationary phase. J Bacteriol 181(1):270–283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soboh F, Khoury AE, Zamboni AC, Davidson D, Mittelman MW (1995) Effects of ciprofloxacin and protamine sulfate combinations against catheter-associated Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 39(6):1281–1286. https://doi.org/10.1128/aac.39.6.1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soderstrom B, Daley DO, Duggin IG (2021) Dynamic localisation of DamX regulates bacterial filamentation and division during UPEC dispersal from host cells. bioRxiv. https://doi.org/10.1101/2021.12.17.473257

  • Söderström B, Pittorino MJ, Daley DO, Duggin IG (2022) Assembly dynamics of FtsZ and DamX during infection-related filamentation and division in uropathogenic E. coli. Nat Commun 13. https://doi.org/10.1038/s41467-022-31378-1

  • Songkiatisak P, Ding F, Cherukuri PK, Xu X-HN (2020) Size-dependent inhibitory effects of antibiotic nanocarriers on filamentation of E. coli. Nanoscale Adv 2(5):2135–2145. https://doi.org/10.1039/C9NA00697D

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soubry N, Wang A, Reyes-Lamothe R (2019) Replisome activity slowdown after exposure to ultraviolet light in Escherichia coli. Proc Natl Acad Sci USA 116(24):11747–11753

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spratt BG (1975) Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc Natl Acad Sci U S A 72(8):2999–3003. https://doi.org/10.1073/pnas.72.8.2999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stackhouse RR, Faith NG, Kaspar CW, Czuprynski CJ, Wong ACL (2012) Survival and virulence of Salmonella enterica serovar enteritidis filaments induced by reduced water activity. Appl Environ Microbiol 78(7):2213–2220. https://doi.org/10.1128/AEM.06774-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steel C, Wan Q, Xu X-HN (2004) Single live cell imaging of chromosomes in chloramphenicol-induced filamentous Pseudomonas aeruginosa. Biochemistry 43(1):175–182. https://doi.org/10.1021/bi035341e

    Article  CAS  PubMed  Google Scholar 

  • Sutton MD, Smith BT, Godoy VG, Walker GC (2000) The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu Rev Genet 34:479–497

    CAS  PubMed  Google Scholar 

  • Szabo R, Štofanı́ková V, (2002) Presence of organic sources of nitrogen is critical for filament formation and pH-dependent morphogenesis in Yarrowia lipolytica. FEMS Microbiol Lett 206(1):45–50

    CAS  PubMed  Google Scholar 

  • Szewczak‐Harris A, Wagstaff J, Löwe J (2019) Cryo‐EM structure of the Min CD copolymeric filament from Pseudomonas aeruginosa at 3.1 Å resolution. FEBS letters 593(15):1915–1926

  • Szwedziak P, Wang Q, Bharat TA, Tsim M, Löwe J (2014) Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. Elife 3:e04601

    PubMed  PubMed Central  Google Scholar 

  • Tétart F, Bouché JP (1992) Regulation of the expression of the cell-cycle gene ftsZ by DicF antisense RNA. Division does not require a fixed number of FtsZ molecules. Mol Microbiol 6(5):615–20. https://doi.org/10.1111/j.1365-2958.1992.tb01508.x

    Article  PubMed  Google Scholar 

  • Tiaden A, Spirig T, Sahr T, Wälti MA, Boucke K, Buchrieser C, Hilbi H (2010) The autoinducer synthase LqsA and putative sensor kinase LqsS regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ Microbiol 12(5):1243–1259

    CAS  PubMed  Google Scholar 

  • Timoumi A, Guillouet SE, Molina-Jouve C, Fillaudeau L, Gorret N (2018) Impacts of environmental conditions on product formation and morphology of Yarrowia lipolytica. Appl Microbiol Biotechnol 102(9):3831–3848

    CAS  PubMed  Google Scholar 

  • Tonthat NK, Milam SL, Chinnam N, Whitfill T, Margolin W, Schumacher MA (2013) SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc Natl Acad Sci U S A 110(26):10586–10591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tran TD, Ali MA, Lee D, Félix M-A, Luallen RJ (2022) Bacterial filamentation as a mechanism for cell-to-cell spread within an animal host. Nat Commun 13(1):1–11

    Google Scholar 

  • Trastoy R, Manso T, Fernández-García L, Blasco L, Ambroa A, Pérez Del Molino ML, Bou G, García-Contreras R, Wood TK, Tomás M (2018) Mechanisms of bacterial tolerance and persistence in the gastrointestinal and respiratory environments. Clin Microbiol Rev 31(4):e00023–18. https://doi.org/10.1128/cmr.00023-18

  • Trusca D, Scott S, Thompson C, Bramhill D (1998) Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J Bacteriol 180(15):3946–3953. https://doi.org/10.1128/JB.180.15.3946-3953.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Typas A, Banzhaf M, Gross CA, Vollmer W (2011) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10(2):123–136. https://doi.org/10.1038/nrmicro267

    Article  PubMed  PubMed Central  Google Scholar 

  • Ultee E, Ramijan K, Dame RT, Briegel A, Claessen D (2019) Stress-induced adaptive morphogenesis in bacteria. Adv Microb Physiol 74:97–141

    PubMed  Google Scholar 

  • Uruén C, Chopo-Escuin G, Tommassen J, Mainar-Jaime RC, Arenas J (2020) Biofilms as promoters of bacterial antibiotic resistance and tolerance. Antibiotics (basel) 10(1):3. https://doi.org/10.3390/antibiotics10010003

    Article  CAS  PubMed Central  Google Scholar 

  • Uyttendaele M, Grangette C, Rogerie F, Pasteau S, Debevere J, Lange M (1998) Influence of cold stress on the preliminary enrichment time needed for detection of enterohemorrhagic Escherichia coli in ground beef by PCR. Appl Environ Microbiol 64(5):1640–1643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uzoechi SC, Abu-Lail NI (2019a) Changes in cellular elasticities and conformational properties of bacterial surface biopolymers of multidrug-resistant Escherichia coli (MDR-E. coli) strains in response to ampicillin. Cell Surf 5:100019. https://doi.org/10.1016/j.tcsw.2019.100019

  • Uzoechi SC, Abu-Lail NI (2019) The effects of β-Lactam antibiotics on surface modifications of multidrug-resistant Escherichia coli: a multiscale approach. Microsc Microanal 25(1):135–150

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uzoechi SC, Abu-Lail NI (2020) Variations in the morphology, mechanics and adhesion of persister and resister E. coli cells in response to ampicillin: AFM study. Antibiotics (Basel) 9(5):235. https://doi.org/10.3390/antibiotics9050235

  • Van Den Ent F, Johnson CM, Persons L, De Boer P, Löwe J (2010) Bacterial actin MreB assembles in complex with cell shape protein RodZ. The EMBO J 29(6):1081–1090

    PubMed  Google Scholar 

  • van Teeseling MCF, de Pedro MA, Cava F (2017) Determinants of bacterial morphology: from fundamentals to possibilities for antimicrobial targeting. Front Microbiol 8:1264.https://doi.org/10.3389/fmicb.2017.01264

  • Wadhawan S, Gautam S (2019) Rescue of Escherichia coli cells from UV-induced death and filamentation by caspase-3 inhibitor. Int Microbiol 22(3):369–376. https://doi.org/10.1007/s10123-019-00060-w

    Article  CAS  PubMed  Google Scholar 

  • Waisbren SJ, Hurley DJ, Waisbren BA (1980) Morphological expressions of antibiotic synergism against Pseudomonas aeruginosa as observed by scanning electron microscopy. Antimicrob Agents Chemother 18(6):969–975. https://doi.org/10.1128/aac.18.6.969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Yu X, Li M, Sun G, Zou L, Li T, Hou L, Guo Y, Shen D, Qu D, Cheng X, Chen L (2019) Filamentation initiated by Cas2 and its association with the acquisition process in cells. Int J Oral Sci 11(3):29. https://doi.org/10.1038/s41368-019-0063-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webb M (1953) Effects of magnesium on cellular division in bacteria. Science 118(3073):607–611. https://doi.org/10.1126/science.118.3073.607

    Article  CAS  PubMed  Google Scholar 

  • Weiss DS, Pogliano K, Carson M, Guzman LM, Fraipont C, Nguyen-Distèche M, Losick R, Beckwith J (1997) Localization of the Escherichia coli cell division protein FtsI (PBP3) to the division site and cell pole. Mol Microbiol 25(4):671–681

    CAS  PubMed  Google Scholar 

  • Wilke MS, Lovering AL, Strynadka NC (2005) β-Lactam antibiotic resistance: a current structural perspective. Curr Opin Microbiol 8(5):525–533

    CAS  PubMed  Google Scholar 

  • Wills AP, Chan EC (1978) Morphogenetic expression of Arthrobacter globiformis 425 in continuous culture with carbon or biotin limitation. Can J Microbiol 24(1):28–30. https://doi.org/10.1139/m78-005

    Article  CAS  PubMed  Google Scholar 

  • Wolf A, Krämer R, Morbach S (2003) Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol Microbiol 49(4):1119–1134

    CAS  PubMed  Google Scholar 

  • Wortinger MA, Quardokus EM, Brun YV (1998) Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus. Mol Microbiol 29(4):963–973

    CAS  PubMed  Google Scholar 

  • Wright JB, Costerton JW, McCoy WF (1988) Filamentous growth of Pseudomonas aeruginosa. J Ind Microbiol 3(3):139–146. https://doi.org/10.1007/BF01569520

    Article  Google Scholar 

  • Wucher BR, Bartlett TM, Hoyos M, Papenfort K, Persat A, Nadell CD (2019) Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms. Proc Natl Acad Sci U S A 116(28):14216–14221. https://doi.org/10.1073/pnas.1819016116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaki S, Kawai Y, Yamazaki K (2021) Long filamentous state of Listeria monocytogenes induced by sublethal sodium chloride stress poses risk of rapid increase in colony-forming units. Food Control 124:107860

    CAS  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208(15):2819–2830

    CAS  PubMed  Google Scholar 

  • Yang DC, Blair KM, Salama NR (2016) Staying in shape: the impact of cell shape on bacterial survival in diverse environments. Microbiol Mol Biol Rev 80(1):187–203

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon MY, Lee KM, Park Y, Yoon SS (2011) Contribution of cell elongation to the biofilm formation of Pseudomonas aeruginosa during anaerobic respiration. PLoS ONE 6(1):e16105. https://doi.org/10.1371/journal.pone.0016105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young KD (2007) Bacterial morphology: why have different shapes? Curr Opin Microbiol 10(6):596–600

    PubMed  PubMed Central  Google Scholar 

  • Zahir T, Wilmaerts D, Franke S, Weytjens B, Camacho R, Marchal K, Hofkens J, Fauvart M, Michiels J (2020) Image-based dynamic phenoty** reveals genetic determinants of filamentation-mediated β-lactam tolerance. Front Microbiol 11:374

    PubMed  PubMed Central  Google Scholar 

  • Zhao S, Zhang Q, Hao G, Liu X, Zhao J, Chen Y, Zhang H, Chen W (2014) The protective role of glycine betaine in Lactobacillus plantarum ST-III against salt stress. Food Control 44:208–213

    CAS  Google Scholar 

Download references

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) grant funded by the Ministry of Education (2021R1A6A1A03039211 and 2022R1A2B5B01001998).

Author information

Author notes

  1. Fazlurrahman Khan and Geum-Jae Jeong equally contributed.

Authors and Affiliations

  1. Marine Integrated Biomedical Technology Center, The National Key Research Institutes in Universities, Pukyong National University, Busan, 48513, Republic of Korea

    Fazlurrahman Khan & Young-Mog Kim

  2. Research Center for Marine Integrated Bionics Technology, Pukyong National University, Busan, 48513, Republic of Korea

    Fazlurrahman Khan & Young-Mog Kim

  3. Department of Food Science and Technology, Pukyong National University, Busan, 48513, Republic of Korea

    Geum-Jae Jeong & Young-Mog Kim

  4. Industry 4.0 Convergence Bionics Engineering, Pukyong National University, Busan, 48513, Republic of Korea

    Nazia Tabassum

  5. Department of Biotechnology, Division of Research and Development, Lovely Professional University, Phagwara, Punjab, 144001, India

    Akanksha Mishra

Authors
  1. Fazlurrahman Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geum-Jae Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nazia Tabassum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akanksha Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Young-Mog Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FK conceptualized the idea, collected the literature, drafted, and reviewed the manuscript. GJJ collected data, wrote, and reviewed the manuscript. NT collected data and wrote the manuscript. AM collected the data and wrote the manuscript. YMK supervision, funding, writing, and editing. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Fazlurrahman Khan or Young-Mog Kim.

Ethics declarations

Ethics approval

This review paper does not contain any studies with human participants or animals.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, F., Jeong, GJ., Tabassum, N. et al. Filamentous morphology of bacterial pathogens: regulatory factors and control strategies. Appl Microbiol Biotechnol 106, 5835–5862 (2022). https://doi.org/10.1007/s00253-022-12128-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-022-12128-1

Keywords

Search

Navigation