Abstract
Initially dismissed as artifacts during sample preparation or as cell debris in bacterial cultures, outer membrane vesicles (OMVs) are now widely accepted as facsimiles of the outer membrane naturally secreted by Gram-negative bacteria. Within the last decades, several studies focused on OMV biogenesis resulting in different, in part complementary models to explain OMV release. Notably, vesicle formation seems to be an essential process as neither a bacterial species nor a mutant lacking vesicle release has been reported so far. Based on the complex physiological roles discussed for OMVs, it is likely that parallel strategies for their production have evolved to ensure their release in diverse conditions. Although, we are still far from a comprehensive mechanistic understanding of OMV release, several studies shed some insights in the processes driving the liberation of OMVs from the bacterial surface. Within this chapter, we will discuss the observations resulting in the current models for OMV formation including their regulation and relevance for bacterial physiology.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aschtgen MS, Lynch JB, Koch E, Schwartzman J, McFall-Ngai M, Ruby E (2016) Rotation of Vibrio fischeri flagella produces outer membrane vesicles that induce host development. J Bacteriol 198(16):2156–2165. https://doi.org/10.1128/JB.00101-16
Baarda BI, Zielke RA, Le Van A, Jerse AE, Sikora AE (2019) Neisseria gonorrhoeae MlaA influences gonococcal virulence and membrane vesicle production. PLoS Pathog 15(3):e1007385. https://doi.org/10.1371/journal.ppat.1007385
Bauwens A, Kunsmann L, Karch H, Mellmann A, Bielaszewska M (2017a) Antibiotic-mediated modulations of outer membrane vesicles in Enterohemorrhagic Escherichia coli O104:H4 and O157:H7. Antimicrob Agents Chemother 61(9):e00937–e00917. https://doi.org/10.1128/AAC.00937-17
Bauwens A, Kunsmann L, Marejkova M, Zhang W, Karch H, Bielaszewska M, Mellmann A (2017b) Intrahost milieu modulates production of outer membrane vesicles, vesicle-associated Shiga toxin 2a and cytotoxicity in Escherichia coli O157:H7 and O104:H4. Environ Microbiol Rep 9(5):626–634. https://doi.org/10.1111/1758-2229.12562
Bernadac A, Gavioli M, Lazzaroni JC, Raina S, Lloubes R (1998) Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180(18):4872–4878
Bonnington KE, Kuehn MJ (2016) Outer membrane vesicle production facilitates LPS remodeling and outer membrane maintenance in Salmonella during environmental transitions. mBio 7(5):e01532-16. https://doi.org/10.1128/mBio.01532-16
Borneleit P, Hermsdorf T, Claus R, Walther P, Kleber HP (1988) Effect of hexadecane-induced vesiculation on the outer membrane of Acinetobacter calcoaceticus. J Gen Microbiol 134(7):1983–1992
Braun V (1975) Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim Biophys Acta 415(3):335–377
Braun V, Rehn K (1969) Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur J Biochem 10(3):426–438
Brennan CA, Hunt JR, Kremer N, Krasity BC, Apicella MA, McFall-Ngai MJ, Ruby EG (2014) A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide. elife 3:e01579. https://doi.org/10.7554/eLife.01579
Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3(3):238–250. https://doi.org/10.1038/nrmicro1098
Brozek KA, Raetz CR (1990) Biosynthesis of lipid A in Escherichia coli. Acyl carrier protein-dependent incorporation of laurate and myristate. J Biol Chem 265(26):15410–15417
Byvalov AA, Malkova MA, Chernyad’ev AV, Dudina LG, Litvinets SG, Martinson EA (2018) Influence of specific bacteriophage on the level of vesicle formation and morphology of cells of Yersinia pseudotuberculosis. Bull Exp Biol Med 165(3):403–407. https://doi.org/10.1007/s10517-018-4180-0
Carpenter CD, Cooley BJ, Needham BD, Fisher CR, Trent MS, Gordon V, Payne SM (2014) The Vps/VacJ ABC transporter is required for intercellular spread of Shigella flexneri. Infect Immun 82(2):660–669. https://doi.org/10.1128/IAI.01057-13
Cascales E, Lloubes R (2004) Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol Microbiol 51(3):873–885
Casjens S (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49(2):277–300
Chang TW, Lin YM, Wang CF, Liao YD (2012) Outer membrane lipoprotein Lpp is Gram-negative bacterial cell surface receptor for cationic antimicrobial peptides. J Biol Chem 287(1):418–428. https://doi.org/10.1074/jbc.M111.290361
Choi HI, Kim M, Jeon J, Han JK, Kim KS (2017) Overexpression of MicA induces production of OmpC-enriched outer membrane vesicles that protect against Salmonella challenge. Biochem Biophys Res Commun 490(3):991–996. https://doi.org/10.1016/j.bbrc.2017.06.152
Clavel T, Germon P, Vianney A, Portalier R, Lazzaroni JC (1998) TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29(1):359–367
Deatherage BL, Cookson BT (2012) Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 80(6):1948–1957. https://doi.org/10.1128/IAI.06014-11
Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT (2009) Biogenesis of bacterial membrane vesicles. Mol Microbiol 72(6):1395–1407
Devos S, Van Putte W, Vitse J, Van Driessche G, Stremersch S, Van Den Broek W, Raemdonck K, Braeckmans K, Stahlberg H, Kudryashev M, Savvides SN, Devreese B (2017) Membrane vesicle secretion and prophage induction in multidrug-resistant Stenotrophomonas maltophilia in response to ciprofloxacin stress. Environ Microbiol 19(10):3930–3937. https://doi.org/10.1111/1462-2920.13793
Duperthuy M, Sjostrom AE, Sabharwal D, Damghani F, Uhlin BE, Wai SN (2013) Role of the Vibrio cholerae matrix protein Bap1 in cross-resistance to antimicrobial peptides. PLoS Pathog 9(10):e1003620. https://doi.org/10.1371/journal.ppat.1003620
Dutta S, Iida K, Takade A, Meno Y, Nair GB, Yoshida S (2004) Release of Shiga toxin by membrane vesicles in Shigella dysenteriae serotype 1 strains and in vitro effects of antimicrobials on toxin production and release. Microbiol Immunol 48(12):965–969
Elhenawy W, Bording-Jorgensen M, Valguarnera E, Haurat MF, Wine E, Feldman MF (2016) LPS remodeling triggers formation of outer membrane vesicles in Salmonella. mBio 7(4):e00940-16. https://doi.org/10.1128/mBio.00940-16
Feiner R, Argov T, Rabinovich L, Sigal N, Borovok I, Herskovits AA (2015) A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 13(10):641–650. https://doi.org/10.1038/nrmicro3527
Ferooz J, Letesson JJ (2010) Morphological analysis of the sheathed flagellum of Brucella melitensis. BMC Res Notes 3:333. https://doi.org/10.1186/1756-0500-3-333
Fuerst JA, Perry JW (1988) Demonstration of lipopolysaccharide on sheathed flagella of Vibrio cholerae O:1 by protein A-gold immunoelectron microscopy. J Bacteriol 170(4):1488–1494
Geis G, Suerbaum S, Forsthoff B, Leying H, Opferkuch W (1993) Ultrastructure and biochemical studies of the flagellar sheath of Helicobacter pylori. J Med Microbiol 38(5):371–377. https://doi.org/10.1099/00222615-38-5-371
Gerding MA, Ogata Y, Pecora ND, Niki H, de Boer PA (2007) The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol Microbiol 63(4):1008–1025. https://doi.org/10.1111/j.1365-2958.2006.05571.x
Gerritzen MJH, Martens DE, Uittenbogaard JP, Wijffels RH, Stork M (2019) Sulfate depletion triggers overproduction of phospholipids and the release of outer membrane vesicles by Neisseria meningitidis. Sci Rep 9(1):4716. https://doi.org/10.1038/s41598-019-41233-x
Gunn JS (2001) Bacterial modification of LPS and resistance to antimicrobial peptides. J Endotoxin Res 7(1):57–62
Gunn JS, Lim KB, Krueger J, Kim K, Guo L, Hackett M, Miller SI (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27:1171–1182
Gwozdzinski K (2018) Macromolecular modification of the cell wall of Gram-negative bacteria leading to antibiotic resistance and formation of outer membrane vesicles. Justus-Liebig-Universität Gießen, Gießen
Hagemann S, Stoger L, Kappelmann M, Hassl I, Ellinger A, Velimirov B (2014) DNA-bearing membrane vesicles produced by Ahrensia kielensis and Pseudoalteromonas marina. J Basic Microbiol 54(10):1062–1072. https://doi.org/10.1002/jobm.201300376
Hampton CM, Guerrero-Ferreira RC, Storms RE, Taylor JV, Yi H, Gulig PA, Wright ER (2017) The opportunistic pathogen Vibrio vulnificus produces outer membrane vesicles in a spatially distinct manner related to capsular polysaccharide. Front Microbiol 8:2177. https://doi.org/10.3389/fmicb.2017.02177
Hankins JV, Madsen JA, Giles DK, Brodbelt JS, Trent MS (2012) Amino acid addition to Vibrio cholerae LPS establishes a link between surface remodeling in gram-positive and gram-negative bacteria. Proc Natl Acad Sci U S A 109(22):8722–8727
Haurat MF, Aduse-Opoku J, Rangarajan M, Dorobantu L, Gray MR, Curtis MA, Feldman MF (2011) Selective sorting of cargo proteins into bacterial membrane vesicles. J Biol Chem 286(2):1269–1276. https://doi.org/10.1074/jbc.M110.185744
Hayashi J, Hamada N, Kuramitsu HK (2002) The autolysin of Porphyromonas gingivalis is involved in outer membrane vesicle release. FEMS Microbiol Lett 216(2):217–222
Hayden JD, Ades SE (2008) The extracytoplasmic stress factor, sigmaE, is required to maintain cell envelope integrity in Escherichia coli. PLoS One 3(2):e1573. https://doi.org/10.1371/journal.pone.0001573
Hoekstra D, van der Laan JW, de Leij L, Witholt B (1976) Release of outer membrane fragments from normally growing Escherichia coli. Biochim Biophys Acta 455(3):889–899
Horstman AL, Kuehn MJ (2000) Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J Biol Chem 275(17):12489–12496
Iwami J, Murakami Y, Nagano K, Nakamura H, Yoshimura F (2007) Further evidence that major outer membrane proteins homologous to OmpA in Porphyromonas gingivalis stabilize bacterial cells. Oral Microbiol Immunol 22(5):356–360
Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177(14):3998–4008
Kadurugamuwa JL, Beveridge TJ (1997) Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J Antimicrob Chemother 40(5):615–621
Kadurugamuwa JL, Clarke AJ, Beveridge TJ (1993) Surface action of gentamicin on Pseudomonas aeruginosa. J Bacteriol 175(18):5798–5805
Kawasaki K, Ernst RK, Miller SI (2004a) 3-O-deacylation of lipid A by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J Biol Chem 279(19):20044–20048. https://doi.org/10.1074/jbc.M401275200
Kawasaki K, Ernst RK, Miller SI (2004b) Deacylation and palmitoylation of lipid A by Salmonellae outer membrane enzymes modulate host signaling through Toll-like receptor 4. J Endotoxin Res 10(6):439–444. https://doi.org/10.1179/096805104225006264
Kulp AJ, Sun B, Ai T, Manning AJ, Orench-Rivera N, Schmid AK, Kuehn MJ (2015) Genome-wide assessment of outer membrane vesicle production in Escherichia coli. PLoS One 10(9):e0139200. https://doi.org/10.1371/journal.pone.0139200
Lam JS, Taylor VL, Islam ST, Hao Y, Kocincova D (2011) Genetic and functional diversity of Pseudomonas aeruginosa lipopolysaccharide. Front Microbiol 2:118. https://doi.org/10.3389/fmicb.2011.00118
Lazzaroni JC, Germon P, Ray MC, Vianney A (1999) The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177(2):191–197
Llamas MA, Ramos JL, Rodriguez-Herva JJ (2000) Mutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J Bacteriol 182(17):4764–4772
Macdonald IA, Kuehn MJ (2013) Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J Bacteriol 195(13):2971–2981. https://doi.org/10.1128/JB.02267-12
Mahalakshmi S, Sunayana MR, SaiSree L, Reddy M (2014) yciM is an essential gene required for regulation of lipopolysaccharide synthesis in Escherichia coli. Mol Microbiol 91(1):145–157. https://doi.org/10.1111/mmi.12452
Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proc Natl Acad Sci U S A 106(19):8009–8014. https://doi.org/10.1073/pnas.0903229106
Manning AJ, Kuehn MJ (2011) Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol 11:258. https://doi.org/10.1186/1471-2180-11-258
Maredia R, Devineni N, Lentz P, Dallo SF, Yu J, Guentzel N, Chambers J, Arulanandam B, Haskins WE, Weitao T (2012) Vesiculation from Pseudomonas aeruginosa under SOS. TheScientificWorldJournal 2012:402919. https://doi.org/10.1100/2012/402919
Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437(7057):422–425. https://doi.org/10.1038/nature03925
Mashburn-Warren L, Howe J, Garidel P, Richter W, Steiniger F, Roessle M, Brandenburg K, Whiteley M (2008) Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol Microbiol 69(2):491–502
Mathur J, Davis BM, Waldor MK (2007) Antimicrobial peptides activate the Vibrio cholerae sigmaE regulon through an OmpU-dependent signalling pathway. Mol Microbiol 63(3):848–858
McBroom AJ, Kuehn MJ (2007) Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63(2):545–558
McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ (2006) Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188(15):5385–5392
McCaig WD, Koller A, Thanassi DG (2013) Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J Bacteriol 195(6):1120–1132. https://doi.org/10.1128/JB.02007-12
McMahon HT, Boucrot E (2015) Membrane curvature at a glance. J Cell Sci 128(6):1065–1070. https://doi.org/10.1242/jcs.114454
Millikan DS, Ruby EG (2004) Vibrio fischeri flagellin A is essential for normal motility and for symbiotic competence during initial squid light organ colonization. J Bacteriol 186(13):4315–4325. https://doi.org/10.1128/JB.186.13.4315-4325.2004
Mitra S, Sinha R, Mitobe J, Koley H (2016) Development of a cost-effective vaccine candidate with outer membrane vesicles of a tolA-disrupted Shigella boydii strain. Vaccine 34(15):1839–1846. https://doi.org/10.1016/j.vaccine.2016.02.018
Moon DC, Choi CH, Lee JH, Choi CW, Kim HY, Park JS, Kim SI, Lee JC (2012) Acinetobacter baumannii outer membrane protein A modulates the biogenesis of outer membrane vesicles. J Microbiol 50(1):155–160. https://doi.org/10.1007/s12275-012-1589-4
Moore RA, Hancock RE (1986) Involvement of outer membrane of Pseudomonas cepacia in aminoglycoside and polymyxin resistance. Antimicrob Agents Chemother 30(6):923–926. https://doi.org/10.1128/aac.30.6.923
Murphy K, Park AJ, Hao Y, Brewer D, Lam JS, Khursigara CM (2014) Influence of O polysaccharides on biofilm development and outer membrane vesicle biogenesis in Pseudomonas aeruginosa PAO1. J Bacteriol 196(7):1306–1317. https://doi.org/10.1128/JB.01463-13
Nakao R, Ramstedt M, Wai SN, Uhlin BE (2012) Enhanced biofilm formation by Escherichia coli LPS mutants defective in Hep biosynthesis. PLoS One 7(12):e51241. https://doi.org/10.1371/journal.pone.0051241
Niehus E, Ye F, Suerbaum S, Josenhans C (2002) Growth phase-dependent and differential transcriptional control of flagellar genes in Helicobacter pylori. Microbiology 148(Pt 12):3827–3837. https://doi.org/10.1099/00221287-148-12-3827
Pal RR, Baidya AK, Mamou G, Bhattacharya S, Socol Y, Kobi S, Katsowich N, Ben-Yehuda S, Rosenshine I (2019) Pathogenic E. coli extracts nutrients from infected host cells utilizing injectisome components. Cell 177(3):683–696 e618. https://doi.org/10.1016/j.cell.2019.02.022
Palva AM (1983) ompA gene in the detection of Escherichia coli and other Enterobacteriaceae by nucleic acid sandwich hybridization. J Clin Microbiol 18(1):92–100
Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, Vogel J (2006) SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62(6):1674–1688
Paramonov N, Bailey D, Rangarajan M, Hashim A, Kelly G, Curtis MA, Hounsell EF (2001) Structural analysis of the polysaccharide from the lipopolysaccharide of Porphyromonas gingivalis strain W50. Eur J Biochem 268(17):4698–4707
Paramonov N, Rangarajan M, Hashim A, Gallagher A, Aduse-Opoku J, Slaney JM, Hounsell E, Curtis MA (2005) Structural analysis of a novel anionic polysaccharide from Porphyromonas gingivalis strain W50 related to Arg-gingipain glycans. Mol Microbiol 58(3):847–863. https://doi.org/10.1111/j.1365-2958.2005.04871.x
Parsons LM, Lin F, Orban J (2006) Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45(7):2122–2128. https://doi.org/10.1021/bi052227i
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(6):1874–1881. https://doi.org/10.1128/AEM.03657-12
Pirbadian S, Barchinger SE, Leung KM, Byun HS, Jangir Y, Bouhenni RA, Reed SB, Romine MF, Saffarini DA, Shi L, Gorby YA, Golbeck JH, El-Naggar MY (2014) Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc Natl Acad Sci U S A 111(35):12883–12888. https://doi.org/10.1073/pnas.1410551111
Prieto AI, Ramos-Morales F, Casadesus J (2006) Repair of DNA damage induced by bile salts in Salmonella enterica. Genetics 174(2):575–584. https://doi.org/10.1534/genetics.106.060889
Qin Z, Lin WT, Zhu S, Franco AT, Liu J (2016) Imaging the motility and chemotaxis machineries in Helicobacter pylori by cryo-electron tomography. J Bacteriol 199:e00695–e00616. https://doi.org/10.1128/JB.00695-16
Raetz CR, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in Gram-negative bacteria. Annu Rev Biochem 76:295–329. https://doi.org/10.1146/annurev.biochem.76.010307.145803
Raivio TL (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56(5):1119–1128. https://doi.org/10.1111/j.1365-2958.2005.04625.x
Rangarajan M, Aduse-Opoku J, Paramonov N, Hashim A, Bostanci N, Fraser OP, Tarelli E, Curtis MA (2008) Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J Bacteriol 190(8):2920–2932. https://doi.org/10.1128/JB.01868-07
Remis JP, Wei D, Gorur A, Zemla M, Haraga J, Allen S, Witkowska HE, Costerton JW, Berleman JE, Auer M (2014) Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ Microbiol 16(2):598–610. https://doi.org/10.1111/1462-2920.12187
Roier S, Zingl FG, Cakar F, Durakovic S, Kohl P, Eichmann TO, Klug L, Gadermaier B, Weinzerl K, Prassl R, Lass A, Daum G, Reidl J, Feldman MF, Schild S (2016) A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria. Nat Commun 7:10515. https://doi.org/10.1038/ncomms10515
Ruhal R, Antti H, Rzhepishevska O, Boulanger N, Barbero DR, Wai SN, Uhlin BE, Ramstedt M (2015) A multivariate approach to correlate bacterial surface properties to biofilm formation by lipopolysaccharide mutants of Pseudomonas aeruginosa. Colloids Surf B Biointerfaces 127:182–191. https://doi.org/10.1016/j.colsurfb.2015.01.030
Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4(1):57–66. https://doi.org/10.1038/nrmicro1322
Sabra W, Lunsdorf H, Zeng AP (2003) Alterations in the formation of lipopolysaccharide and membrane vesicles on the surface of Pseudomonas aeruginosa PAO1 under oxygen stress conditions. Microbiology 149(Pt 10):2789–2795. https://doi.org/10.1099/mic.0.26443-0
Salkinoja-Salonen M, Nurmiaho EL (1978) The effect of lipopolysaccharide composition on the ultrastructure of Pseudomonas aeruginosa. J Gen Microbiol 105(1):23–28. https://doi.org/10.1099/00221287-105-1-23
Sampath V, McCaig WD, Thanassi DG (2018) Amino acid deprivation and central carbon metabolism regulate the production of outer membrane vesicles and tubes by Francisella. Mol Microbiol 107(4):523–541. https://doi.org/10.1111/mmi.13897
Samsudin F, Ortiz-Suarez ML, Piggot TJ, Bond PJ, Khalid S (2016) OmpA: a flexible clamp for bacterial cell wall attachment. Structure 24(12):2227–2235. https://doi.org/10.1016/j.str.2016.10.009
Schertzer JW, Whiteley M (2012) A bilayer-couple model of bacterial outer membrane vesicle biogenesis. mBio 3(2):e00297-11. https://doi.org/10.1128/mBio.00297-11
Schertzer JW, Whiteley M (2013) Bacterial outer membrane vesicles in trafficking, communication and the host-pathogen interaction. J Mol Microbiol Biotechnol 23(1–2):118–130. https://doi.org/10.1159/000346770
Schwechheimer C, Kuehn MJ (2013) Synthetic effect between envelope stress and lack of outer membrane vesicle production in Escherichia coli. J Bacteriol 195(18):4161–4173. https://doi.org/10.1128/JB.02192-12
Schwechheimer C, Sullivan CJ, Kuehn MJ (2013) Envelope control of outer membrane vesicle production in Gram-negative bacteria. Biochemistry 52(18):3031–3040. https://doi.org/10.1021/bi400164t
Schwechheimer C, Kulp A, Kuehn MJ (2014) Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC Microbiol 14:324. https://doi.org/10.1186/s12866-014-0324-1
Shen L, Gao X, Wei J, Chen L, Zhao X, Li B, Duan K (2012) PA2800 plays an important role in both antibiotic susceptibility and virulence in Pseudomonas aeruginosa. Curr Microbiol 65(5):601–609. https://doi.org/10.1007/s00284-012-0196-2
Shetty A, Hickey WJ (2014) Effects of outer membrane vesicle formation, surface-layer production and nanopod development on the metabolism of phenanthrene by Delftia acidovorans Cs1-4. PLoS One 9(3):e92143. https://doi.org/10.1371/journal.pone.0092143
Shetty A, Chen S, Tocheva EI, Jensen GJ, Hickey WJ (2011) Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles. PLoS One 6(6):e20725. https://doi.org/10.1371/journal.pone.0020725
Simmons LA, Foti JJ, Cohen SE, Walker GC (2008) The SOS Regulatory Network. EcoSal Plus 3(1). https://doi.org/10.1128/ecosalplus.5.4.3
Song T, Mika F, Lindmark B, Liu Z, Schild S, Bishop A, Zhu J, Camilli A, Johansson J, Vogel J, Wai SN (2008) A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol Microbiol 70(1):100–111
Sonntag I, Schwarz H, Hirota Y, Henning U (1978) Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J Bacteriol 136(1):280–285
Storm DR, Rosenthal KS, Swanson PE (1977) Polymyxin and related peptide antibiotics. Annu Rev Biochem 46:723–763. https://doi.org/10.1146/annurev.bi.46.070177.003451
Suzuki H, Nishimura Y, Yasuda S, Nishimura A, Yamada M, Hirota Y (1978) Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope. Mol Gen Genet 167(1):1–9
Suzuki T, Murai T, Fukuda I, Tobe T, Yoshikawa M, Sasakawa C (1994) Identification and characterization of a chromosomal virulence gene, vacJ, required for intercellular spreading of Shigella flexneri. Mol Microbiol 11(1):31–41
Sych T, Mely Y, Romer W (2018) Lipid self-assembly and lectin-induced reorganization of the plasma membrane. Philos Trans R Soc Lond Ser B Biol Sci 373(1747):20170117. https://doi.org/10.1098/rstb.2017.0117
Taheri N, Mahmud A, Sandblad L, Fallman M, Wai SN, Fahlgren A (2018) Campylobacter jejuni bile exposure influences outer membrane vesicles protein content and bacterial interaction with epithelial cells. Sci Rep 8(1):16996. https://doi.org/10.1038/s41598-018-35409-0
Tarahovsky YS, Ivanitsky GR, Khusainov AA (1994) Lysis of Escherichia coli cells induced by bacteriophage T4. FEMS Microbiol Lett 122(1–2):195–199. https://doi.org/10.1111/j.1574-6968.1994.tb07164.x
Tashiro Y, Sakai R, Toyofuku M, Sawada I, Nakajima-Kambe T, Uchiyama H, Nomura N (2009) Outer membrane machinery and alginate synthesis regulators control membrane vesicle production in Pseudomonas aeruginosa. J Bacteriol 191(24):7509–7519
Tashiro Y, Ichikawa S, Nakajima-Kambe T, Uchiyama H, Nomura N (2010) Pseudomonas quinolone signal affects membrane vesicle production in not only gram-negative but also gram-positive bacteria. Microbes Environ 25(2):120–125. https://doi.org/10.1264/jsme2.me09182
Tashiro Y, Inagaki A, Shimizu M, Ichikawa S, Takaya N, Nakajima-Kambe T, Uchiyama H, Nomura N (2011) Characterization of phospholipids in membrane vesicles derived from Pseudomonas aeruginosa. Biosci Biotechnol Biochem 75(3):605–607
Toyofuku M, Zhou S, Sawada I, Takaya N, Uchiyama H, Nomura N (2014) Membrane vesicle formation is associated with pyocin production under denitrifying conditions in Pseudomonas aeruginosa PAO1. Environ Microbiol 16(9):2927–2938. https://doi.org/10.1111/1462-2920.12260
Toyofuku M, Carcamo-Oyarce G, Yamamoto T, Eisenstein F, Hsiao CC, Kurosawa M, Gademann K, Pilhofer M, Nomura N, Eberl L (2017) Prophage-triggered membrane vesicle formation through peptidoglycan damage in Bacillus subtilis. Nat Commun 8(1):481. https://doi.org/10.1038/s41467-017-00492-w
Trent MS, Pabich W, Raetz CR, Miller SI (2001) A PhoP/PhoQ-induced lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J Biol Chem 276(12):9083–9092. https://doi.org/10.1074/jbc.M010730200
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. https://doi.org/10.1038/ncomms11220
Turner L, Praszkier J, Hutton ML, Steer D, Ramm G, Kaparakis-Liaskos M, Ferrero RL (2015) Increased outer membrane vesicle formation in a Helicobacter pylori tolB mutant. Helicobacter 20(4):269–283. https://doi.org/10.1111/hel.12196
Udekwu KI, Wagner EG (2007) Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res 35(4):1279–1288. https://doi.org/10.1093/nar/gkl1154
Urashima A, Sanou A, Yen H, Tobe T (2017) Enterohaemorrhagic Escherichia coli produces outer membrane vesicles as an active defence system against antimicrobial peptide LL-37. Cell Microbiol 19(11). https://doi.org/10.1111/cmi.12758
Vollmer W, Bertsche U (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778(9):1714–1734. https://doi.org/10.1016/j.bbamem.2007.06.007
Wang Y (2002) The function of OmpA in Escherichia coli. Biochem Biophys Res Commun 292(2):396–401. https://doi.org/10.1006/bbrc.2002.6657
Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28(2):127–181. https://doi.org/10.1016/j.femsre.2003.08.001
Wensink J, Witholt B (1981) Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur J Biochem 116(2):331–335
Yeh YC, Comolli LR, Downing KH, Shapiro L, McAdams HH (2010) The Caulobacter Tol-Pal complex is essential for outer membrane integrity and the positioning of a polar localization factor. J Bacteriol 192(19):4847–4858. https://doi.org/10.1128/JB.00607-10
Zavan L, Bitto NJ, Johnston EL, Greening DW, Kaparakis-Liaskos M (2019) Helicobacter pylori growth stage determines the size, protein composition, and preferential cargo packaging of outer membrane vesicles. Proteomics 19(1–2):e1800209. https://doi.org/10.1002/pmic.201800209
Zhao L, Gao X, Liu C, Lv X, Jiang N, Zheng S (2017) Deletion of the vacJ gene affects the biology and virulence in Haemophilus parasuis serovar 5. Gene 603:42–53. https://doi.org/10.1016/j.gene.2016.12.009
Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7(1):9–19. https://doi.org/10.1038/nrm1784
Acknowledgements
This work was supported by the BioTechMed-Graz Flagship Project SECRETOME to S.S, the Austrian FWF grants P25691 to S.S., P27654 to S.S., and W901-B12 (DK Molecular Enzymology) to F.G.Z. and S.S.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Zingl, F.G., Leitner, D.R., Schild, S. (2020). Biogenesis of Gram-Negative OMVs. In: Kaparakis-Liaskos, M., Kufer, T. (eds) Bacterial Membrane Vesicles. Springer, Cham. https://doi.org/10.1007/978-3-030-36331-4_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-36331-4_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-36330-7
Online ISBN: 978-3-030-36331-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)