Skip to main content

Advertisement

SpringerLink
Log in

Release mechanisms and molecular interactions of Pseudomonas aeruginosa extracellular DNA

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

Abstract

Pseudomonas aeruginosa infection is a significant threat for clinicians. Increasing incidents of resistant biofilm infection result in high mortality rates worldwide. There is a considerable current interest in the field of extracellular DNA (eDNA)–mediated P. aeruginosa biofilm formation. eDNA acts as a glue to make biofilm more stable. This review focuses on the diverse mechanisms and factors, which enhance the eDNA release into the extracellular milieu. Furthermore, eDNA-mediated molecular interactions within the biofilm are emphasized. In addition, drug resistance mechanisms due to the versatility of eDNA are discussed. Spatial physiological diversity is expected due to different metabolic activity of bacterial subpopulation present in P. aeruginosa biofilm layers. In P. aeruginosa, eDNA release is accomplished by cell lysis and OMVs (outer membrane vesicles). eDNA release is a spontaneous and multifactorial process, which may be accomplished by PQS, pyocyanin, and lambda prophage induction. Hydrogen peroxide and pyocin trigger cell death, which may facilitate eDNA release. Lung mucosa of cystic fibrosis patients is enriched with eDNA, which acidifies biofilm and develops P. aeruginosa resistance to aminoglycosides. Further studies on spatial and molecular characterization of bacterial subpopulation in biofilm will shed light on eDNA-biofilm interaction more precisely.

Key Points

• Extracellular DNA (eDNA) is a key component of Pseudomonas aeruginosa biofilm.

• P. aeruginosa eDNA acts as a glue to make biofilm more stronger.

• Bacterial cell death or lysis may be the potential way to release P. aeruginosa eDNA into extracellular milieu.

• P. aeruginosa eDNA contributes to develop resistance to antimicrobials.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alipour M, Suntres ZE, Omri A (2009) Importance of DNase and alginate lyase for enhancing free and liposome encapsulatedaminoglycoside activity against Pseudomonas aeruginosa. J Antimicrob Chemother 64:317–325

  • Alkawash MA, Soothill JS, Schiller NL (2006) Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS 114:131–138

    CAS  PubMed  Google Scholar 

  • Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T (2006) Characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128

    CAS  PubMed  Google Scholar 

  • Allocati N, Masulli M, Di Ilio C, De Laurenzi V (2015) Die for the community: an overview of programmed cell death in bacteria. Cell Death Dis 6:e1609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ascher J, Ceccherini MT, Pantani OL, Agnelli A, Borgogni F, Guerri G, Nannipieri P, Pietramellara G (2009) Sequential extraction and genetic fingerprinting of a forest soil metagenome. Appl Soil Ecol 42:176–181

    Google Scholar 

  • Aspe M, Jensen L, Melegrito J, Sun M (2012) The role of alginate and extracellular DNA in biofilm-meditated Pseudomonas aeruginosa gentamicin resistance. J Exp Microbiol Immunol 16:42–48

    Google Scholar 

  • Bahamondez-Canas TF, Heersema LA, Smyth HDC (2019) Current status of in vitro models and assays for susceptibility testing for wound biofilm infections. Biomedicines 7. https://doi.org/10.3390/biomedicines7020034

  • Banin E, Brady KM, Greenberg EP (2006) Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol 72:2064–2069

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barken KB, Pamp SJ, Yang L, Gjermansen M, Bertrand JJ, Klausen M, Givskov M, Whitchurch CB, Engel JN, Tolker-Nielsen T (2008) Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10:2331–2343

    CAS  PubMed  Google Scholar 

  • Bassetti M, Righi E, Viscoli C (2008) Pseudomonas aeruginosa serious infections: mono or combination antimicrobial therapy? Curr Med Chem 15:517–522

    CAS  PubMed  Google Scholar 

  • Beaumont PE, McHugh B, Gwyer Findlay E, Mackellar A, Mackenzie KJ, Gallo RL, Govan JR, Simpson AJ, Davidson DJ (2014) Cathelicidin host defence peptide augments clearance of pulmonary Pseudomonas aeruginosa infection by its influence on neutrophil function in vivo. PLoS One 9:e99029

    PubMed  PubMed Central  Google Scholar 

  • Beringer PM, Vinks AA, Jelliffe RW, Shapiro BJ (2000) Pharmacokinetics of tobramycin in adults with cystic fibrosis: implications for once-daily administration. Antimicrob Agents Chemother 44:809–813

    CAS  PubMed  PubMed Central  Google Scholar 

  • Binnenkade L, Teichmann L, Thormann KM (2014) Iron triggers λSo prophage induction and release of extracellular DNA in Shewanella oneidensisMR-1 biofilms. Appl Environ Microbiol 80:5304–5316

    PubMed  PubMed Central  Google Scholar 

  • Bitto NJ, Chapman R, Pidot S, Costin A, Lo C, Choi J, D'Cruze T, Reynolds EC, Dashper SG, Turnbull L, Whitchurch CB, Stinear TP, Stacey KJ, Ferrero RL (2017) Bacterial membrane vesicles transport their DNA cargo into host cells. Sci Rep 7:7072

    PubMed  PubMed Central  Google Scholar 

  • Blackledge MS, Worthington RJ, Melander C (2013) Biologically inspired strategies for combating bacterial biofilms. Curr Opin Pharmacol 13:699–706

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA (2009) Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5:e1000382

    PubMed  PubMed Central  Google Scholar 

  • Brasseur R, Laurent G, Ruysschaert JM, Tulkens P (1984) Interactions of aminoglycoside antibiotics with negatively charged lipid layers. Biochemical and conformational studies. Biochem Pharmacol 33:629–637

    CAS  PubMed  Google Scholar 

  • Busscher HJ, Norde W, van der Mei HC (2008) Specific molecular recognition and nonspecific contributions to bacterial interaction forces. Appl Environ Microbiol 74:2559–2564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carrolo M, Frias MJ, Pinto FR, Melo-Cristino J, Ramirez M (2010) Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae. PLoS One 5:e15678

    CAS  PubMed  PubMed Central  Google Scholar 

  • Centers for Disease Control and Prevention (2013) Pseudomonas aeruginosa in healthcare settings. Healthcare-associated infections. https://www.cdc.gov/hai/organisms/pseudomonas.html

  • Centers for Disease Control and Prevention (2018) Biggest threats and data. Antibiotic / antimicrobial resistance (AR / AMR) https://www.cdc.gov/drugresistance/biggest_threats.html?CDC_AA_refVal=https%3A%2F%2Fwww.cdc.gov%2Fdrugresistance%2Fthreat-report-2013%2Findex.html

  • Chen F, Chen G, Liu Y, Jin Y, Cheng Z, Liu Y, Yang L, Jin S, Wu W (2017) Pseudomonas aeruginosa oligoribonuclease contributes to tolerance to ciprofloxacin by regulating pyocin biosynthesis. Antimicrob Agents Chemother 61

  • Chiang WC, Nilsson M, Jensen PO, Hoiby N, Nielsen TE, Givskov M, Tolker-Nielsen T (2013) Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 57:2352–2361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Christie PJ (2001) Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol Microbiol 40:294–305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ciofu O, Tolker-Nielsen T (2019) Tolerance and resistance of Pseudomonas aeruginosa biofilms to antimicrobial agents-how P. aeruginosa can escape antibiotics. Front Microbiol 10:913

    PubMed  PubMed Central  Google Scholar 

  • Cirz RT, O'Neill BM, Hammond JA, Head SR, Romesberg FE (2006) Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J Bacteriol 188:7101–7110

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cooke AC, Nello AV, Ernst RK, Schertzer JW (2019) Analysis of Pseudomonas aeruginosa biofilm membrane vesicles supports multiple mechanisms of biogenesis. PLoS One 14:e0212275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    CAS  PubMed  Google Scholar 

  • Das T, Manefield M (2012) Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLoS One 7:e46718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das T, Sharma PK, Busscher HJ, van der Mei HC, Krom BP (2010) Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microbiol 76:3405–3408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das T, Kutty SK, Kumar N, Manefield M (2013) Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS One 8:e58299

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das T, Sehar S, Koop L, Wong YK, Ahmed S, Siddiqui KS, Manefield M (2014) Influence of calcium in extracellular DNA mediated bacterial aggregation and biofilm formation. PLoS One 9:e91935

    PubMed  PubMed Central  Google Scholar 

  • Dauros-Singorenko P, Blenkiron C, Phillips A, Swift S (2018) The functional RNA cargo of bacterial membrane vesicles. FEMS Microbiol Lett 365. https://doi.org/10.1093/femsle/fny023

  • Davies CB, Harrison MD, Huygens F (2017) Pseudomonas aeruginosa Trent and zinc homeostasis. FEMS Microbiol Lett 364. https://doi.org/10.1093/femsle/fnx151

  • Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT (2009) Biogenesis of bacterial membrane vesicles. Mol Microbiol 72:1395–1407

    CAS  PubMed  PubMed Central  Google Scholar 

  • DeLeon S, Clinton A, Fowler H, Everett J, Horswill AR, Rumbaugh KP (2014) Synergistic interactions of Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro wound model. Infect Immun 82:4718–4728

    PubMed  PubMed Central  Google Scholar 

  • Deziel E, Lepine F, Milot S, He J, Mindrinos MN, Tompkins RG, Rahme LG (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci U S A 101:1339–1344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Domenech M, Garcia E (2018) Autolysin-independent DNA release in Streptococcus pneumoniae in vitro biofilms. bioRxiv. https://doi.org/10.1101/322818

  • Duport C, Baysse C, Michel-Briand Y (1995) Molecular characterization of pyocin S3, a novel S-type pyocin from Pseudomonas aeruginosa. J Biol Chem 270:8920–8927

    CAS  PubMed  Google Scholar 

  • Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189:7945–7947

    CAS  PubMed  PubMed Central  Google Scholar 

  • Folsom JP, Richards L, Pitts B, Roe F, Ehrlich GD, Parker A, Mazurie A, Stewart PS (2010) Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol 10:294

    PubMed  PubMed Central  Google Scholar 

  • Frederiksen B, Pressler T, Hansen A, Koch C, Hoiby N (2006) Effect of aerosolized rhDNase (Pulmozyme) on pulmonary colonization in patients with cystic fibrosis. Acta Paediatr 95:1070–1074

    PubMed  Google Scholar 

  • Fuxman Bass JI, Gabelloni ML, Alvarez ME, Vermeulen ME, Russo DM, Zorreguieta A, Geffner JR, Trevani AS (2008) Characterization of bacterial DNA binding to human neutrophil surface. Lab Investig 88:926–937

    CAS  PubMed  Google Scholar 

  • Fuxman Bass JI, Russo DM, Gabelloni ML, Geffner JR, Giordano M, Catalano M, Zorreguieta A, Trevani AS (2010) Extracellular DNA: a major proinflammatory component of Pseudomonas aeruginosa biofilms. J Immunol 184:6386–6395

    CAS  PubMed  Google Scholar 

  • Ghafoor A, Hay ID, Rehm BH (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghoul M, West SA, Johansen HK, Molin S, Harrison OB, Maiden MCJ, Jelsbak L, Bruce JB, Griffin AS. (2015) Bacteriocin mediated competition in cystic fibrosis lung infections Proc Biol sci 282. https://doi.org/10.1098/rspb.2015.0972

  • Gi M, Lee KM, Kim SC, Yoon JH, Yoon SS, Choi JY (2015) A novel siderophore system is essential for the growth of Pseudomonas aeruginosa in airway mucus. Sci Rep 5:14644

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gloag ES, Turnbull L, Huang A, Vallotton P, Wang H, Nolan LM, Mililli L, Hunt C, Lu J, Osvath SR, Monahan LG, Cavaliere R, Charles IG, Wand MP, Gee ML, Prabhakar R, Whitchurch CB (2013) Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci U S A 110:11541–11546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grande R, Di Marcantonio MC, Robuffo I, Pompilio A, Celia C, Di Marzio L, Paolino D, Codagnone M, Muraro R, Stoodley P, Hall-Stoodley L, Mincione G (2015) Helicobacter pylori ATCC 43629/NCTC 11639 outer membrane vesicles (OMVs) from biofilm and planktonic phase associated with extracellular DNA (eDNA). Front Microbiol 6:1369

    PubMed  PubMed Central  Google Scholar 

  • Gutu AD, Rodgers NS, Park J, Moskowitz SM (2015) Pseudomonas aeruginosa high-level resistance to polymyxins and other antimicrobial peptides requires cprA, a gene that is disrupted in the PAO1 strain. Antimicrob Agents Chemother 59:5377–5387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hall CW, Mah TF (2017) Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 41:276–301

    CAS  PubMed  Google Scholar 

  • Halverson TW, Wilton M, Poon KK, Petri B, Lewenza S (2015) DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog 11:e1004593

    PubMed  PubMed Central  Google Scholar 

  • Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT, Dillard JP (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55:1704–1721

    CAS  PubMed  Google Scholar 

  • Haussler S, Becker T (2008) The pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLoS Pathog 4:e1000166

    PubMed  PubMed Central  Google Scholar 

  • Hazan R, Sat B, Engelberg-Kulka H (2004) Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J Bacteriol 186:3663–3669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hazan R, Que YA, Maura D, Strobel B, Majcherczyk PA, Hopper LR, Wilbur DJ, Hreha TN, Barquera B, Rahme LG (2016) Auto poisoning of the respiratory chain by a quorum-sensing-regulated molecule favors biofilm formation and antibiotic tolerance. Curr Biol 26:195–206

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heacock-Kang Y, Sun Z, Zarzycki-Siek J, McMillan IA, Norris MH, Bluhm AP, Cabanas D, Fogen D, Vo H, Donachie SP, Borlee BR, Sibley CD, Lewenza S, Schurr MJ, Schweizer HP, Hoang TT (2017) Spatial transcriptomes within the Pseudomonas aeruginosa biofilm architecture. Mol Microbiol 106:976–985

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hentzer M, Teitzel GM, Balzer GJ, Heydorn A, Molin S, Givskov M (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183:5395–5401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins S, Heeb S, Rampioni G, Fletcher MP, Williams P, Camara M (2018) Differential regulation of the phenazine biosynthetic operons by quorum sensing in Pseudomonas aeruginosa PAO1-N. Front Cell Infect Microbiol 8:252

    PubMed  PubMed Central  Google Scholar 

  • Hoiby N, Ciofu O, Bjarnsholt T (2010) Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 5:1663–1674

    CAS  PubMed  Google Scholar 

  • Hotterbeekx A, Kumar-Singh S, Goossens H, Malhotra-Kumar S (2017) In vivo and in vitro interactions between Pseudomonas aeruginosa and Staphylococcus spp. Front Cell Infect Microbiol 7:106

    PubMed  PubMed Central  Google Scholar 

  • Ibanez de Aldecoa AL, Zafra O, Gonzalez-Pastor JE (2017) Mechanisms and regulation of extracellular DNA release and its biological roles in microbial communities. Front Microbiol 8:1390

    PubMed  PubMed Central  Google Scholar 

  • Irie Y, Roberts AEL, Kragh KN, Gordon VD, Hutchison J, Allen RJ, Melaugh G, Bjarnsholt T, West SA, Diggle SP (2017) The Pseudomonas aeruginosa PSL polysaccharide is a social but noncheatable trait in biofilms. MBio. https://doi.org/10.1128/mBio.00374-17

  • Jack AA, Khan S, Powell LC, Pritchard MF, Beck K, Sadh H, Sutton L, Cavaliere A, Florance H, Rye PD, Thomas DW, Hill KE (2018) Alginate oligosaccharide-induced modification of the lasI-lasR and rhlI-rhlR quorum-sensing systems in Pseudomonas aeruginosa. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.02318-17

  • Jakubovics NS, Shields RC, Rajarajan N, Burgess JG (2013) Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 57:467–475

    CAS  PubMed  Google Scholar 

  • Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS, Sadovskaya I (2015) Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proc Natl Acad Sci U S A 112:11353–11358

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson L, Horsman SR, Charron-Mazenod L, Turnbull AL, Mulcahy H, Surette MG, Lewenza S (2013) Extracellular DNA-induced antimicrobial peptide resistance in Salmonella enterica serovar Typhimurium. BMC Microbiol 13:115

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones CJ, Wozniak DJ (2017) Psl produced by mucoid Pseudomonas aeruginosa contributes to the establishment of biofilms and immune evasion. MBio

  • Jurcisek JA, Brockman KL, Novotny LA, Goodman SD, Bakaletz LO (2017) Nontypeable Haemophilus influenzae releases DNA and DNABII proteins via a T4SS-like complexand ComE of the type IV pilus machinery. Proc Natl Acad Sci U S A 114:E6632–E6641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kovacha KN, Flemingb D, Rumbaughb KP, Gordon VD (2019) Specific disruption of established P. aeruginosa biofilms using polymer-attacking enzymes. bioRxiv. https://doi.org/10.1101/598979

  • Kreth J, Vu H, Zhang Y, Herzberg MC (2009) Characterization of hydrogen peroxide-induced DNA release by Streptococcus sanguinis and Streptococcus gordonii. J Bacteriol 191:6281–6291

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuehn MJ, Kesty NC (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19:2645–2655

    CAS  PubMed  Google Scholar 

  • Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Ann Rev Microbiol 64:163–184

    CAS  Google Scholar 

  • Kumar S, Kolodkin-Gal I, Engelberg-Kulka H (2013) Novel quorum-sensing peptides mediating interspecies bacterial cell death. MBio 4:e00314–e00313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lamppa JW, Ackerman ME, Lai JI, Scanlon TC, Griswold KE (2011) Genetically engineered alginate lyase-PEG conjugates exhibit enhanced catalytic function and reduced immunoreactivity. PLoS One 6:e17042

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JY, Ko KS (2014) Mutations and expression of PmrAB and PhoPQ related with colistin resistance in Pseudomonas aeruginosa clinical isolates. Diagn Microb Infect Dis 78:271–276

    CAS  Google Scholar 

  • Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41

    CAS  PubMed  Google Scholar 

  • LeRoux M, Kirkpatrick RL, Montauti EI, Tran BQ, Peterson SB, Harding BN, Whitney JC, Russell AB, Traxler B, Goo YA, Goodlett DR, Wiggins PA, Mougous JD (2015) Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa. Elife 4:e05701

    PubMed Central  Google Scholar 

  • Lewenza S (2013) Extracellular DNA-induced antimicrobial peptide resistance mechanisms in Pseudomonas aeruginosa. Front Microbiol 4:21

    PubMed  PubMed Central  Google Scholar 

  • Liao S, Klein MI, Heim KP, Fan Y, Bitoun JP, Ahn SJ, Burne RA, Koo H, Brady LJ, Wen ZT (2014) Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J Bacteriol 196:2355–2366

    PubMed  PubMed Central  Google Scholar 

  • Lin X, Han F, Yang Z, Lu X-z, Yu W-g (2006) A novel alginate lyase 844 with high activity on acetylated alginate of Pseudomonas aeruginosa FRD1 845 from Pseudomonas sp. QD03. World J Microbiol Biotechnol 22:81–88

    Google Scholar 

  • Ma Q, Zhai Y, Schneider JC, Ramseier TM, Saier MH Jr (2003) Protein secretion systems of Pseudomonas aeruginosa and P fluorescens. Biochim Biophys Acta 1611:223–233

    CAS  PubMed  Google Scholar 

  • Ma L, Conover M, Lu H, Parsek MR, Bayles K, Wozniak DJ (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5:e1000354

    PubMed  PubMed Central  Google Scholar 

  • Malhotra S, Limoli DH, English AE, Parsek MR, Wozniak DJ (2018) Mixed communities of mucoid and nonmucoid Pseudomonas aeruginosa exhibit enhanced resistance to host antimicrobials. MBio

  • Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36:893–916

    CAS  PubMed  Google Scholar 

  • Martinez-Aleman SR, Campos-Garcia L, Palma-Nicolas JP, Hernandez-Bello R, Gonzalez GM, Sanchez-Gonzalez A (2017) Understanding the entanglement: neutrophil extracellular traps (NETs) in cystic fibrosis. Fron Cell Infect Microbiol 7:104

    Google Scholar 

  • Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422–425

    CAS  PubMed  Google Scholar 

  • Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–6465

    CAS  PubMed  PubMed Central  Google Scholar 

  • McFarland KA, Dolben EL, LeRoux M, Kambara TK, Ramsey KM, Kirkpatrick RL, Mougous JD, Hogan DA, Dove SL (2015) A self-lysis pathway that enhances the virulence of a pathogenic bacterium. Proc Natl Acad Sci U S A 112:8433–8438

    CAS  PubMed  PubMed Central  Google Scholar 

  • Michel-Briand Y, Baysse C (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84:499–510

    CAS  PubMed  Google Scholar 

  • Miller AK, Brannon MK, Stevens L, Johansen HK, Selgrade SE, Miller SI, Hoiby N, Moskowitz SM (2011) PhoQ mutations promote lipid A modification and polymyxin resistance of Pseudomonas aeruginosa found in colistin-treated cystic fibrosis patients. Antimicrob Agents Chemother 55:5761–5769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minandri F, Imperi F, Frangipani E, Bonchi C, Visaggio D, Facchini M, Pasquali P, Bragonzi A, Visca P (2016) Role of iron uptake systems in Pseudomonas aeruginosa virulence and airway infection. Infect Immun 84:2324–2335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra M, Byrd MS, Sergeant S, Azad AK, Parsek MR, McPhail L, Schlesinger LS, Wozniak DJ (2012) Pseudomonas aeruginosa Psl polysaccharide reduces neutrophil phagocytosis and the oxidativeresponse by limiting complement-mediated opsonization. Cell Microbiol 14:95–106

    CAS  PubMed  Google Scholar 

  • Mo CY, Manning SA, Roggiani M, Culyba MJ, Samuels AN, Sniegowski PD, Goulian M, Kohli RM (2016) Systematically altering bacterial SOS activity under stress reveals therapeutic strategies for potentiating antibiotics. mSphere

  • Moradali MF, Ghods S, Rehm BH (2017) Pseudomonas aeruginosa lifestyle: a paradigm for adaptation, survival, and persistence. Front Cell Infect Microbiol 7:39

    PubMed  PubMed Central  Google Scholar 

  • Moreau-Marquis S, O'Toole GA, Stanton BA (2009) Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells. Am J Respir Cell Mol Biol 41:305–313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4:e1000213

    PubMed  PubMed Central  Google Scholar 

  • Nair HA, Periasamy S, Yang L, Kjelleberg S, Rice SA (2017) Real time, spatial, and temporal mapping of the distribution of c-di-GMP during biofilm development. J Biol Chem 292:477–487

    CAS  PubMed  Google Scholar 

  • Nakamura S, Higashiyama Y, Izumikawa K, Seki M, Kakeya H, Yamamoto Y, Yanagihara K, Miyazaki Y, Mizuta Y, Kohno S (2008) The roles of the quorum-sensing system in the release of extracellular DNA, lipopolysaccharide, and membrane vesicles from Pseudomonas aeruginosa. Jpn J Infect Dis 61:375–378

    CAS  PubMed  Google Scholar 

  • Nakao R, Myint SL, Wai SN, Uhlin BE (2018) Enhanced biofilm formation and membrane vesicle release by Escherichia coli expressing a commonly occurring plasmid gene, kil. Front Microbiol 9:2605

    PubMed  PubMed Central  Google Scholar 

  • Nakayama K, Takashima K, Ishihara H, Shinomiya T, Kageyama M, Kanaya S, Ohnishi M, Murata T, Mori H, Hayashi T (2000) The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol 38:213–231

    CAS  PubMed  Google Scholar 

  • Nguyen AT, O'Neill MJ, Watts AM, Robson CL, Lamont IL, Wilks A, Oglesby-Sherrouse AG (2014) Adaptation of iron homeostasis pathways by a Pseudomonas aeruginosa pyoverdine mutant in the cystic fibrosis lung. J Bacteriol 196:2265–2276

    PubMed  PubMed Central  Google Scholar 

  • Nichols DP, Durmowicz AG, Field A, Flume PA, VanDevanter DR, Mayer-Hamblett N (2019) Developing inhaled antibiotics in cystic fibrosis: current challenges and opportunities. Ann Am Thorac Soc 16:534–539

    PubMed  PubMed Central  Google Scholar 

  • O'Brien S, Fothergill JL (2017) The role of multispecies social interactions in shaping Pseudomonas aeruginosa pathogenicity in the cystic fibrosis lung. FEMS Microbiol Lett 364. https://doi.org/10.1093/femsle/fnx128

  • O'Malley YQ, Reszka KJ, Spitz DR, Denning GM, Britigan BE (2004) Pseudomonas aeruginosa pyocyanin directly oxidizes glutathione and decreases its levels in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 287:L94–L103

  • Pallett R, Leslie LJ, Lambert PA, Milic I, Devitt A, Marshall LJ (2019) Anaerobiosis influences virulence properties of Pseudomonas aeruginosa cystic fibrosis isolatesand the interaction with Staphylococcus aureus. Sci Rep 9:6748

    PubMed  PubMed Central  Google Scholar 

  • Palmgren R, Nielsen PH (1996) Accumulation of DNA in the exopolymeric matrix of activated sludge and bacterial cultures. Water Sci Technol 34:233–240

    CAS  Google Scholar 

  • Penterman J, Singh PK, Walker GC (2014) Biological cost of pyocin production during the SOS response in Pseudomonas aeruginosa. J Bacteriol 196:3351–3359

    PubMed  PubMed Central  Google Scholar 

  • Perez-Cruz C, Carrion O, Delgado L, Martinez G, Lopez-Iglesias C, Mercade E (2013) New type of outer membrane vesicle produced by the gram-negative bacterium Shewanella vesiculosa M7T: implications for DNA content. Appl Environ Microbiol 79:1874–1881

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petrova OE, Sauer K (2016) Escaping the biofilm in more than one way: desorption, detachment or dispersion. Curr Opin Microbiol 30:67–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Price-Whelan A, Dietrich LEP, Newman DK (2006) Rethinking secondary metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78

    CAS  PubMed  Google Scholar 

  • Puca V, Ercolino E, Celia C, Bologna G, Di Marzio L, Mincione G, Marchisio M, Miscia S, Muraro R, Lanuti P, Grande R (2019) Detection and quantification of eDNA-associated bacterial membrane vesicles by flow cytometry. Int J Mol Sci 20. https://doi.org/10.3390/ijms20215307

  • Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083–2092

    CAS  PubMed  Google Scholar 

  • Rasamiravaka T, Labtani Q, Duez P, El Jaziri M (2015) The formation of biofilms by Pseudomonas aeruginosa: a review of the natural and synthetic compounds interfering with control mechanisms. Biomed Res Int 2015:759348

    PubMed  PubMed Central  Google Scholar 

  • Recinos DA, Sekedat MD, Hernandez A, Cohen TS, Sakhtah H, Prince AS, Price-Whelan A, Dietrich LE (2012) Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc Natl Acad Sci U S A 109:19420–19425

    CAS  PubMed  PubMed Central  Google Scholar 

  • Redero M, Lopez-Causape C, Aznar J, Oliver A, Blazquez J, Prieto AI (2018) Susceptibility to R-pyocins of Pseudomonas aeruginosa clinical isolates from cystic fibrosispatients. J Antimicrob Chemother 73:2770–2776

    CAS  PubMed  Google Scholar 

  • Reichhardt C, Parsek MR (2019) Confocal laser scanning microscopy for analysis of Pseudomonas aeruginosa biofilm architecture and matrix localization. Front Microbiol 10:677

    PubMed  PubMed Central  Google Scholar 

  • Reid DW, Carroll V, O'May C, Champion A, Kirov SM (2007) Increased airway iron as a potential factor in the persistence of Pseudomonas aeruginosa infection in cystic fibrosis. Eur Respir J 30:286–292

    CAS  PubMed  Google Scholar 

  • Renelli M, Matias V, Lo RY, Beveridge TJ (2004) DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150:2161–2169

    CAS  PubMed  Google Scholar 

  • Rice KC, Bayles KW (2008) Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72:85–109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rubin BK (2014) Secretion properties, clearance, and therapy in airway disease. Translat Respir Med 2:6

    Google Scholar 

  • Sano Y, Kageyama M (1981) Purification and properties of an S-type pyocin, pyocin AP41. J Bacteriol 146:733–739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Savari M, Rostami S, Ekrami A, Bahador A (2016) Characterization of toxin-antitoxin (TA) systems in Pseudomonas aeruginosa clinical isolates in Iran. Jundishapur J Microbiol 9:e26627

    PubMed  PubMed Central  Google Scholar 

  • Schurek KN, Sampaio JL, Kiffer CR, Sinto S, Mendes CM, Hancock RE (2009) Involvement of pmrAB and phoPQ in polymyxin B adaptation and inducible resistance in non-cystic fibrosis clinical isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother 53:4345–4351

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schurr MJ (2013) Which bacterial biofilm exopolysaccharide is preferred, Psl or alginate? J Bacteriol 195:1623–1626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schuster M, Sexton DJ, Diggle SP, Greenberg EP (2013) Acyl-homoserine lactone quorum sensing: from evolution to application. Ann Rev Microbiol 67:43–63

    CAS  Google Scholar 

  • Serra DO, Hengge R (2014) Stress responses go three dimensional - the spatial order of physiological differentiation in bacterial macrocolony biofilms. Environ Microbiol 16:1455–1471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skopelja-Gardner S, Theprungsirikul J, Lewis KA, Hammond JH, Carlson KM, Hazlett HF, Nymon A, Nguyen D, Berwin BL, Hogan DA, Rigby WFC (2019) Regulation of Pseudomonas aeruginosa-mediated neutrophil extracellular traps. Front Immunol 10:1670

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith K, Martin L, Rinaldi A, Rajendran R, Ramage G, Walker D (2012) Activity of pyocin S2 against Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 56:1599–1601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steichen CT, Cho C, Shao JQ, Apicella MA (2011) The Neisseria gonorrhoeae biofilm matrix contains DNA, and an endogenous nuclease controls its incorporation. Infect Immun 79:1504–15011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tahrioui A, Duchesne R, Bouffartigues E, Rodrigues S, Maillot O, Tortuel D, Hardouin J, Taupin L, Groleau MC, Dufour A, Deziel E, Brenner-Weiss G, Feuilloley M, Orange N, Lesouhaitier O, Cornelis P, Chevalier S (2019) Extracellular DNA release, quorum sensing, and PrrF1/F2 small RNAs are key players in Pseudomonas aeruginosa tobramycin-enhanced biofilm formation. NPJ Biofilms Microbiomes 5:15

    PubMed  PubMed Central  Google Scholar 

  • Tai KP, Kamdar K, Yamaki J, Le VV, Tran D, Tran P, Selsted ME, Ouellette AJ, Wong-Beringer A (2015) Microbicidal effects of alpha- and theta-defensins against antibiotic-resistant Staphylococcus aureus and Pseudomonas aeruginosa. Innate Immun 21:17–29

    PubMed  Google Scholar 

  • Tanaka M, Kurata T, Fujisawa C, Ohshima Y, Aoki H, Okazaki O, Hakusui H (1993) Mechanistic study of inhibition of levofloxacin absorption by aluminum hydroxide. Antimicrob Agents Chemother 37:2173–2178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang L, Schramm A, Neu TR, Revsbech NP, Meyer RL (2013) Extracellular DNA in adhesion and biofilm formation of four environmental isolates: a quantitative study. FEMS Microbiol Ecol 86:394–403

    CAS  PubMed  Google Scholar 

  • Tashiro Y, Takaki K, Futamata H (2019) Targeted delivery using membrane vesicles in prokaryotes. Biophys Physicobiol 16:114–120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tetz VV, Tetz GV (2010) Effect of extracellular DNA destruction by DNase I on characteristics of forming biofilms. DNA Cell Biol 29:399–405

    CAS  PubMed  Google Scholar 

  • Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190:5690–5698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trevani AS, Chorny A, Salamone G, Vermeulen M, Gamberale R, Schettini J, Raiden S, Geffner J (2003) Bacterial DNA activates human neutrophils by a CpG-independent pathway. Eur J Immunol 33:3164–3174

    CAS  PubMed  Google Scholar 

  • Tseng BS, Zhang W, Harrison JJ, Quach TP, Song JL, Penterman J, Singh PK, Chopp DL, Packman AI, Parsek MR (2013) The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ Microbiol 15:2865–2878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbull L, Toyofuku M, Hynen AL, Kurosawa M, Pessi G, Petty NK, Osvath SR, Carcamo-Oyarce G, Gloag ES, Shimoni R, Omasits U, Ito S, Yap X, Monahan LG, Cavaliere R, Ahrens CH, Charles IG, Nomura N, Eberl L, Whitchurch CB (2016) Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun 7:11220

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vipin C, Mujeeburahiman M, Saptami K, Arun AB, Rekha PD (2019) Synergistic interactions of quercetin with antibiotics against biofilm associated clinical isolates of Pseudomonas aeruginosa in vitro. bioRxiv. https://doi.org/10.1101/601336

  • Waksman G, Fronzes R (2010) Molecular architecture of bacterial type IV secretion systems. Trends Biochem Sci 35:691–698

    CAS  PubMed  Google Scholar 

  • Wang S, Liu X, Liu H, Zhang L, Guo Y, Yu S, Wozniak DJ, Ma LZ (2015) The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ Microbiol Rep 7:330–340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182:2675–2679

    CAS  PubMed  PubMed Central  Google Scholar 

  • Webb JS, Thompson LS, James S, Charlton T, Tolker-Nielsen T, Koch B, Givskov M, Kjelleberg S (2003) Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185:4585–4592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Q, Ma LZ (2013) Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int J Mol Sci 14:20983–21005

    PubMed  PubMed Central  Google Scholar 

  • Weiss G, Carver PL (2018) Role of divalent metals in infectious disease susceptibility and outcome. Clin Microbiol Infect 24:16–23

    CAS  PubMed  Google Scholar 

  • Wessel AK, Liew J, Kwon T, Marcotte EM, Whiteley M (2013) Role of Pseudomonas aeruginosa peptidoglycan-associated outer membrane proteins in vesicle formation. J Bacteriol 195:213–219

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wessel AK, Arshad TA, Fitzpatrick M, Connell JL, Bonnecaze RT, Shear JB, Whiteley M (2014) Oxygen limitation within a bacterial aggregate. MBio 5:e00992

    PubMed  PubMed Central  Google Scholar 

  • Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487

    CAS  PubMed  Google Scholar 

  • Williamson KS, Richards LA, Perez-Osorio AC, Pitts B, McInnerney K, Stewart PS, Franklin MJ (2012) Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernationfactors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 194:2062–2073

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilton M, Charron-Mazenod L, Moore R, Lewenza S (2015) Extracellular DNA acidifies biofilms and induces aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 60:544–553

    PubMed  PubMed Central  Google Scholar 

  • Wilton M, Wong MJQ, Tang L, Liang X, Moore R, Parkins MD, Lewenza S, Dong TG (2016) Chelation of membrane-bound cations by extracellular DNA activates the type VI secretion system in Pseudomonas aeruginosa. Infect Immun 84:2355–2361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilton M, Halverson TWR, Charron-Mazenod L, Parkins MD, Lewenza S (2018) Secreted phosphatase and deoxyribonuclease are required by Pseudomonas aeruginosa to defend against neutrophil extracellular traps. Infect Immun. https://doi.org/10.1128/IAI.00403-18

  • Woith E, Fuhrmann G, Melzig MF (2019) Extracellular vesicles—Connecting kingdoms. Int J Mol Sci 20:5695

  • Wysoczynski-Horita CL, Boursier ME, Hill R, Hansen K, Blackwell HE, Churchill MEA (2018) Mechanism of agonism and antagonism of the Pseudomonas aeruginosa quorum sensing regulator QscR with non-native ligands. Mol Microbiol 108:240–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan S, Wu G (2019) Can biofilm be reversed through quorum sensing in Pseudomonas aeruginosa? Front Microbiol 10:1582

    PubMed  PubMed Central  Google Scholar 

  • Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153:1318–1328

    CAS  PubMed  Google Scholar 

  • Young RL, Malcolm KC, Kret JE, Caceres SM, Poch KR, Nichols DP, Taylor-Cousar JL, Saavedra MT, Randell SH, Vasil ML, Burns JL, Moskowitz SM, Nick JA (2011) Neutrophil extracellular trap (NET)-mediated killing of Pseudomonas aeruginosa: evidence of acquired resistance within the CF airway, independent of CFTR. PLoS One 6:e23637

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zafra O, Lamprecht-Grandio M, de Figueras CG, Gonzalez-Pastor JE (2012) Extracellular DNA release by undomesticated Bacillus subtilis is regulated by early competence. PLoS One 7:e48716

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zemke AC, Bomberger JM (2016) Microbiology: social suicide for a good cause. Curr Biol 26:R80–R82

    CAS  PubMed  Google Scholar 

  • Zhang W, Sun J, Ding W, Lin J, Tian R, Lu L, Liu X, Shen X, Qian PY (2015) Extracellular matrix-associated proteins form an integral and dynamic system during Pseudomonas aeruginosa biofilm development. Front Cell Infect Microbiol 5:40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zweig M, Schork S, Koerdt A, Siewering K, Sternberg C, Thormann K, Albers SV, Molin S, van der Does C (2014) Secreted single-stranded DNA is involved in the initial phase of biofilm formation by Neisseria gonorrhoeae. Environ Microbiol 16:1040–1052

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to express my sincere gratitude to Prof. Chandan K. Sen, Indiana Center for Regenerative Medicine and Engineering, University School of Medicine, Department of Surgery, Indiana University, Indianapolis, IN 46202, USA; and Prof. Daniel Wozniak, Departments of Microbial Infection and Immunity, Microbiology, Center for Microbial Interface Biology, The Ohio State University, Columbus, OH 43210, USA.

Author information

Authors and Affiliations

  1. Department of Surgery, University School of Medicine, Indiana University, Indianapolis, IN, 46202, USA

    Subendu Sarkar

  2. Department of Surgery, Davis Heart and Lung Research Institute, The Ohio State University Wexner Medical Center, Columbus, OH, 43210, USA

    Subendu Sarkar

Authors
  1. Subendu Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SS conceived and designed the research. SS analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Subendu Sarkar.

Ethics declarations

Ethical statement

This study does not contain any work related to human participants or animals.

Conflict of interest

The author declares that there is no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sarkar, S. Release mechanisms and molecular interactions of Pseudomonas aeruginosa extracellular DNA. Appl Microbiol Biotechnol 104, 6549–6564 (2020). https://doi.org/10.1007/s00253-020-10687-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10687-9

Keywords

Search

Navigation