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Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria

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  • Authors: Cécile Berne1, Adrien Ducret2, Gail G. Hardy3, Yves V. Brun4
  • Editors: Mahmoud Ghannoum5, Matthew Parsek6, Marvin Whiteley7, Pranab Mukherjee8
    Affiliations: 1: Department of Biology, Jordan Hall JH142, Indiana University, Bloomington, IN 47405; 2: Department of Biology, Jordan Hall JH142, Indiana University, Bloomington, IN 47405; 3: Department of Biology, Jordan Hall JH142, Indiana University, Bloomington, IN 47405; 4: Department of Biology, Jordan Hall JH142, Indiana University, Bloomington, IN 47405; 5: Case Western Reserve University, Cleveland, OH; 6: University of Washington, Seattle, WA; 7: University of Texas at Austin, Austin, TX; 8: Case Western Reserve University, Cleveland, OH
  • Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
  • Received 20 February 2015 Accepted 03 March 2015 Published 24 July 2015
  • Yves V. Brun, [email protected]
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  • Abstract:

    During the first step of biofilm formation, initial attachment is dictated by physicochemical and electrostatic interactions between the surface and the bacterial envelope. Depending on the nature of these interactions, attachment can be transient or permanent. To achieve irreversible attachment, bacterial cells have developed a series of surface adhesins promoting specific or nonspecific adhesion under various environmental conditions. This article reviews the recent advances in our understanding of the secretion, assembly, and regulation of the bacterial adhesins during biofilm formation, with a particular emphasis on the fimbrial, nonfimbrial, and discrete polysaccharide adhesins in Gram-negative bacteria.

  • Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria. Microbiol Spectrum 3(4):MB-0018-2015. doi:10.1128/microbiolspec.MB-0018-2015.


1. Dunne WM. 2002. Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166. [PubMed][CrossRef]
2. van Oss CJ. 2003. Long-range and short-range mechanisms of hydrophobic attraction and hydrophilic repulsion in specific and aspecific interactions. J Mol Recognit 16:177–190. [PubMed][CrossRef]
3. Stewart RJ. 2011. Protein-based underwater adhesives and the prospects for their biotechnological production. Appl Microbiol Biotechnol 89:27–33. [PubMed][CrossRef]
4. O’Toole G, Kaplan HB, Kolter R. 2000. Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79. [PubMed][CrossRef]
5. Monds RD, O’Toole GA. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol 17:73–87. [PubMed][CrossRef]
6. Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890. [PubMed][CrossRef]
7. Geng J, Henry N. 2011. Short time-scale bacterial adhesion dynamics, p 315–331. In Link D, Goldman A (ed), Bacterial Adhesion. Springer, Dordrecht, The Netherlands. [CrossRef]
8. Beloin C, Roux A, Ghigo J-M. 2008. Escherichia coli biofilms, p 249–289. In Romeo T (ed), Bacterial Biofilms. Springer, Dordrecht, The Netherlands. [PubMed][CrossRef]
9. Karatan E, Watnick P. 2009. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347. [PubMed][CrossRef]
10. Pratt LA, Kolter R. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30:285–293. [CrossRef]
11. Entcheva-Dimitrov P, Spormann AM. 2004. Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus. J Bacteriol 186:8254–8266. [PubMed][CrossRef]
12. Van Houdt R, Michiels CW. 2005. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res Microbiol 156:626–633. [PubMed][CrossRef]
13. Proft T, Baker EN. 2009. Pili in Gram-negative and Gram-positive bacteria: structure, assembly and their role in disease. Cell Mol Life Sci 66:613–635. [PubMed][CrossRef]
14. Burrows LL. 2012. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol 66:493–520. [PubMed][CrossRef]
15. St Geme JW, Pinkner JS, 3rd, Krasan GP, Heuser J, Bullitt E, Smith AL, Hultgren SJ. 1996. Haemophilus influenzae pili are composite structures assembled via the HifB chaperone. Proc Natl Acad Sci USA 93:11913–11918. [PubMed][CrossRef]
16. Gohl O, Friedrich A, Hoppert M, Averhoff B. 2006. The thin pili of Acinetobacter sp. strain BD413 mediate adhesion to biotic and abiotic surfaces. Appl Environ Microbiol 72:1394–1401. [PubMed][CrossRef]
17. Inhulsen S, Aguilar C, Schmid N, Suppiger A, Riedel K, Eberl L. 2012. Identification of functions linking quorum sensing with biofilm formation in Burkholderia cenocepacia H111. Microbiologyopen 1:225–242. [PubMed][CrossRef]
18. Ormeno-Orrillo E, Menna P, Almeida LG, Ollero FJ, Nicolas MF, Pains Rodrigues E, Shigueyoshi Nakatani A, Silva Batista JS, Oliveira Chueire LM, Souza RC, Ribeiro Vasconcelos AT, Megias M, Hungria M, Martinez-Romero E. 2012. Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 which are used in inoculants for common bean ( Phaseolus vulgaris L.). BMC Genomics 13:735. [PubMed][CrossRef]
19. Nuccio SP, Baumler AJ. 2007. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71:551–575. [PubMed][CrossRef]
20. Wurpel DJ, Beatson SA, Totsika M, Petty NK, Schembri MA. 2013. Chaperone-usher fimbriae of Escherichia coli. PLoS One 8:e52835. [PubMed][CrossRef]
21. Busch A, Waksman G. 2012. Chaperone-usher pathways: diversity and pilus assembly mechanism. Philos Trans R Soc Lond B Biol Sci 367:1112–1122. [PubMed][CrossRef]
22. Waksman G, Hultgren SJ. 2009. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7:765–774. [PubMed][CrossRef]
23. Han Z, Pinkner JS, Ford B, Obermann R, Nolan W, Wildman SA, Hobbs D, Ellenberger T, Cusumano CK, Hultgren SJ, Janetka JW. 2010. Structure-based drug design and optimization of mannoside bacterial FimH antagonists. J Med Chem 53:4779–4792. [PubMed][CrossRef]
24. Hertig S, Vogel V. 2012. Catch bonds. Curr Biol 22:R823–R825. [PubMed][CrossRef]
25. Rakshit S, Sivasankar S. 2014. Biomechanics of cell adhesion: how force regulates the lifetime of adhesive bonds at the single molecule level. Phys Chem Chem Phys 16:2211–2223. [PubMed][CrossRef]
26. Liaqat I, Sakellaris H. 2012. Biofilm formation and binding specificities of CFA/I, CFA/II and CS2 adhesions of enterotoxigenic Escherichia coli and Cfae-R181A mutant. Braz J Microbiol 43:969–980. [PubMed][CrossRef]
27. Ammendolia MG, Bertuccini L, Iosi F, Minelli F, Berlutti F, Valenti P, Superti F. 2010. Bovine lactoferrin interacts with cable pili of Burkholderia cenocepacia. Biometals 23:531–542. [PubMed][CrossRef]
28. Sakellaris H, Scott JR. 1998. New tools in an old trade: CS1 pilus morphogenesis. Mol Microbiol 30:681–687. [PubMed][CrossRef]
29. Starks AM, Froehlich BJ, Jones TN, Scott JR. 2006. Assembly of CS1 pili: the role of specific residues of the major pilin, CooA. J Bacteriol 188:231–239. [PubMed][CrossRef]
30. Galkin VE, Kolappan S, Ng D, Zong Z, Li J, Yu X, Egelman EH, Craig L. 2013. The structure of the CS1 pilus of enterotoxigenic Escherichia coli reveals structural polymorphism. J Bacteriol 195:1360–1370. [PubMed][CrossRef]
31. Perez-Casal J, Swartley JS, Scott JR. 1990. Gene encoding the major subunit of CS1 pili of human enterotoxigenic Escherichia coli. Infect Immun 58:3594–3600. [PubMed]
32. Voegele K, Sakellaris H, Scott JR. 1997. CooB plays a chaperone-like role for the proteins involved in formation of CS1 pili of enterotoxigenic Escherichia coli. Proc Natl Acad Sci USA 94:13257–13261. [PubMed][CrossRef]
33. Sakellaris H, Balding DP, Scott JR. 1996. Assembly proteins of CS1 pili of enterotoxigenic Escherichia coli. Mol Microbiol 21:529–541. [PubMed][CrossRef]
34. Froehlich BJ, Karakashian A, Melsen LR, Wakefield JC, Scott JR. 1994. CooC and CooD are required for assembly of CS1 pili. Mol Microbiol 12:387–401. [PubMed][CrossRef]
35. Macfarlane S, Dillon JF. 2007. Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 102:1187–1196. [PubMed][CrossRef]
36. Tomich M, Mohr CD. 2003. Adherence and autoaggregation phenotypes of a Burkholderia cenocepacia cable pilus mutant. FEMS Microbiol Lett 228:287–297. [PubMed][CrossRef]
37. Giltner CL, Nguyen Y, Burrows LL. 2012. Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 76:740–772. [PubMed][CrossRef]
38. Giltner CL, Habash M, Burrows LL. 2010. Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol 398:444–461. [PubMed][CrossRef]
39. Kuchma SL, Griffin EF, O’Toole GA. 2012. Minor pilins of the type IV pilus system participate in the negative regulation of swarming motility. J Bacteriol 194:5388–5403. [PubMed][CrossRef]
40. Johnson MD, Garrett CK, Bond JE, Coggan KA, Wolfgang MC, Redinbo MR. 2011. Pseudomonas aeruginosa PilY1 binds integrin in an RGD- and calcium-dependent manner. PLoS One 6:e29629. doi:10.1371/journal.pone.0029629. [PubMed][CrossRef]
41. Takhar HK, Kemp K, Kim M, Howell PL, Burrows LL. 2013. The platform protein is essential for type IV pilus biogenesis. J Biol Chem 288:9721–9728. [PubMed][CrossRef]
42. Tammam S, Sampaleanu LM, Koo J, Manoharan K, Daubaras M, Burrows LL, Howell PL. 2013. PilMNOPQ from the Pseudomonas aeruginosa type IV pilus system form a transenvelope protein interaction network that interacts with PilA. J Bacteriol 195:2126–2135. [PubMed][CrossRef]
43. Wehbi H, Portillo E, Harvey H, Shimkoff AE, Scheurwater EM, Howell PL, Burrows LL. 2011. The peptidoglycan-binding protein FimV promotes assembly of the Pseudomonas aeruginosa type IV pilus secretin. J Bacteriol 193:540–550. [PubMed][CrossRef]
44. Koo J, Tang T, Harvey H, Tammam S, Sampaleanu L, Burrows LL, Howell PL. 2013. Functional mapping of PilF and PilQ in the Pseudomonas aeruginosa type IV pilus system. Biochemistry 52:2914–2923. [PubMed][CrossRef]
45. O’Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304. [PubMed][CrossRef]
46. Klausen M, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50:61–68. [PubMed][CrossRef]
47. Chiang P, Burrows LL. 2003. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J Bacteriol 185:2374–2378. [PubMed][CrossRef]
48. Watnick PI, Fullner KJ, Kolter R. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol 181:3606–3609. [PubMed]
49. Shime-Hattori A, Iida T, Arita M, Park KS, Kodama T, Honda T. 2006. Two type IV pili of Vibrio parahaemolyticus play different roles in biofilm formation. FEMS Microbiol Lett 264:89–97. [PubMed][CrossRef]
50. Reguera G, Kolter R. 2005. Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J Bacteriol 187:3551–3555. [PubMed][CrossRef]
51. Lutz C, Erken M, Noorian P, Sun S, McDougald D. 2013. Environmental reservoirs and mechanisms of persistence of Vibrio cholerae. Front Microbiol 4:375. [PubMed][CrossRef]
52. Manning PA. 1997. The tcp gene cluster of Vibrio cholerae. Gene 192:63–70. [CrossRef]
53. Bose N, Taylor RK. 2005. Identification of a TcpC-TcpQ outer membrane complex involved in the biogenesis of the toxin-coregulated pilus of Vibrio cholerae. J Bacteriol 187:2225–2232. [PubMed][CrossRef]
54. LaPointe CF, Taylor RK. 2000. The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases. J Biol Chem 275:1502–1510. [PubMed][CrossRef]
55. Tripathi SA, Taylor RK. 2007. Membrane association and multimerization of TcpT, the cognate ATPase ortholog of the Vibrio cholerae toxin-coregulated-pilus biogenesis apparatus. J Bacteriol 189:4401–4409. [PubMed][CrossRef]
56. Tomich M, Planet PJ, Figurski DH. 2007. The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5:363–375. [PubMed][CrossRef]
57. Inoue T, Tanimoto I, Ohta H, Kato K, Murayama Y, Fukui K. 1998. Molecular characterization of low-molecular-weight component protein, Flp, in Actinobacillus actinomycetemcomitans fimbriae. Microbiol Immunol 42:253–258. [PubMed][CrossRef]
58. Kachlany SC, Planet PJ, DeSalle R, Fine DH, Figurski DH. 2001. Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol 9:429–437. [PubMed][CrossRef]
59. Tomich M, Fine DH, Figurski DH. 2006. The TadV protein of Actinobacillus actinomycetemcomitans is a novel aspartic acid prepilin peptidase required for maturation of the Flp1 pilin and TadE and TadF pseudopilins. J Bacteriol 188:6899–6914. [PubMed][CrossRef]
60. Bhattacharjee MK, Kachlany SC, Fine DH, Figurski DH. 2001. Nonspecific adherence and fibril biogenesis by Actinobacillus actinomycetemcomitans: TadA protein is an ATPase. J Bacteriol 183:5927–5936. [PubMed][CrossRef]
61. Perez-Cheeks BA, Planet PJ, Sarkar IN, Clock SA, Xu Q, Figurski DH. 2012. The product of tadZ, a new member of the parA/minD superfamily, localizes to a pole in Aggregatibacter actinomycetemcomitans. Mol Microbiol 83:694–711. [PubMed][CrossRef]
62. Haase EM, Zmuda JL, Scannapieco FA. 1999. Identification and molecular analysis of rough-colony-specific outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect Immun 67:2901–2908. [PubMed]
63. Clock SA, Planet PJ, Perez BA, Figurski DH. 2008. Outer membrane components of the Tad (tight adherence) secreton of Aggregatibacter actinomycetemcomitans. J Bacteriol 190:980–990. [PubMed][CrossRef]
64. Inoue T, Shingaki R, Sogawa N, Sogawa CA, Asaumi J, Kokeguchi S, Fukui K. 2003. Biofilm formation by a fimbriae-deficient mutant of Actinobacillus actinomycetemcomitans. Microbiol Immunol 47:877–881. [PubMed][CrossRef]
65. Saito T, Ishihara K, Ryu M, Okuda K, Sakurai K. 2010. Fimbriae-associated genes are biofilm-forming factors in Aggregatibacter actinomycetemcomitans strains. Bull Tokyo Dent Coll 51:145–150. [PubMed][CrossRef]
66. Skerker JM, Shapiro L. 2000. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 19:3223–3234. [PubMed][CrossRef]
67. Bodenmiller D, Toh E, Brun YV. 2004. Development of surface adhesion in Caulobacter crescentus. J Bacteriol 186:1438–1447. [PubMed][CrossRef]
68. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, Fuqua C, Brun YV. 2012. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol Microbiol 83:41–51. [PubMed][CrossRef]
69. Ruer S, Stender S, Filloux A, de Bentzmann S. 2007. Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J Bacteriol 189:3547–3555. [PubMed][CrossRef]
70. Bednarska NG, Schymkowitz J, Rousseau F, Van Eldere J. 2013. Protein aggregation in bacteria: the thin boundary between functionality and toxicity. Microbiology 159:1795–1806. [PubMed][CrossRef]
71. Dueholm MS, Albertsen M, Otzen D, Nielsen PH. 2012. Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS One 7:e51274. doi:10.1371/journal.pone.0051274. [PubMed][CrossRef]
72. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855. [PubMed][CrossRef]
73. Evans ML, Chapman MR. 2013. Curli biogenesis: order out of disorder. Biochim Biophys Acta [Epub ahead of print.] doi:10.1016/j.bbamcr.2013.09.010. [PubMed][CrossRef]
74. Cookson AL, Cooley WA, Woodward MJ. 2002. The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int J Med Microbiol 292:195–205. [PubMed][CrossRef]
75. Bokranz W, Wang X, Tschape H, Romling U. 2005. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 54:1171–1182. [PubMed][CrossRef]
76. Saldana Z, Xicohtencatl-Cortes J, Avelino F, Phillips AD, Kaper JB, Puente JL, Giron JA. 2009. Synergistic role of curli and cellulose in cell adherence and biofilm formation of attaching and effacing Escherichia coli and identification of Fis as a negative regulator of curli. Environ Microbiol 11:992–1006. [PubMed][CrossRef]
77. Zhou Y, Smith D, Leong BJ, Brannstrom K, Almqvist F, Chapman MR. 2012. Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms. J Biol Chem 287:35092–35103. [PubMed][CrossRef]
78. Gerlach RG, Hensel M. 2007. Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297:401–415. [PubMed][CrossRef]
79. Chagnot C, Zorgani MA, Astruc T, Desvaux M. 2013. Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol 4:303. [PubMed][CrossRef]
80. Delepelaire P. 2004. Type I secretion in Gram-negative bacteria. Biochim Biophys Acta 1694:149–161. [PubMed][CrossRef]
81. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888–2896. [PubMed][CrossRef]
82. Lasa I, Penades JR. 2006. Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157:99–107. [PubMed][CrossRef]
83. Yousef F, Espinosa-Urgel M. 2007. In silico analysis of large microbial surface proteins. Res Microbiol 158:545–550. [PubMed][CrossRef]
84. Espinosa-Urgel M, Salido A, Ramos JL. 2000. Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182:2363–2369. [PubMed][CrossRef]
85. Hinsa SM, Espinosa-Urgel M, Ramos JL, O’Toole GA. 2003. Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49:905–918. [PubMed][CrossRef]
86. Fuqua C. 2010. Passing the baton between laps: adhesion and cohesion in Pseudomonas putida biofilms. Mol Microbiol 77:533–536. [PubMed][CrossRef]
87. El-Kirat-Chatel S, Beaussart A, Boyd CD, O’Toole GA, Dufrêne YF. 2013. Single-cell and single-molecule analysis deciphers the localization, adhesion, and mechanics of the biofilm adhesin LapA. ACS Chem Biol 9:485–494. [PubMed][CrossRef]
88. El-Kirat-Chatel S, Boyd CD, O’Toole GA, Dufrêne YF. 2014. Single-molecule analysis of Pseudomonas fluorescens footprints. ACS Nano 8:1690–1698. [PubMed][CrossRef]
89. Martinez-Gil M, Yousef-Coronado F, Espinosa-Urgel M. 2010. LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Mol Microbiol 77:549–561. [PubMed][CrossRef]
90. Duque E, de la Torre J, Bernal P, Molina-Henares MA, Alaminos M, Espinosa-Urgel M, Roca A, Fernandez M, de Bentzmann S, Ramos JL. 2013. Identification of reciprocal adhesion genes in pathogenic and non-pathogenic Pseudomonas. Environ Microbiol 15:36–48. [PubMed][CrossRef]
91. Valle J, Latasa C, Gil C, Toledo-Arana A, Solano C, Penades JR, Lasa I. 2012. Bap, a biofilm matrix protein of Staphylococcus aureus prevents cellular internalization through binding to GP96 host receptor. PLoS Pathog 8:e1002843. doi:10.1371/journal.ppat.1002843. [PubMed][CrossRef]
92. Wagner C, Hensel M. 2011. Adhesive mechanisms of Salmonella enterica. Adv Exp Med Biol 715:17–34. [PubMed][CrossRef]
93. Wagner C, Polke M, Gerlach RG, Linke D, Stierhof YD, Schwarz H, Hensel M. 2011. Functional dissection of SiiE, a giant non-fimbrial adhesin of Salmonella enterica. Cell Microbiol 13:1286–1301. [PubMed][CrossRef]
94. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T. 2010. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75:815–826. [PubMed][CrossRef]
95. Martinez-Gil M, Quesada JM, Ramos-Gonzalez MI, Soriano MI, de Cristobal RE, Espinosa-Urgel M. 2013. Interplay between extracellular matrix components of Pseudomonas putida biofilms. Res Microbiol 164:382–389. [PubMed][CrossRef]
96. Martínez-Gil M, Ramos-González MI, Espinosa-Urgel M. 2014. Role of c-di-GMP and the Gac system in the transcriptional control of the genes coding for the Pseudomonas putida adhesins LapA and LapF. J Bacteriol 196:1484–1495. [PubMed][CrossRef]
97. Desvaux M, Parham NJ, Henderson IR. 2004. Type V protein secretion: simplicity gone awry? Curr Issues Mol Biol 6:111–124. [PubMed]
98. Bernstein HD. 2007. Are bacterial ‘autotransporters’ really transporters? Trends Microbiol 15:441–447. [PubMed][CrossRef]
99. Leyton DL, Rossiter AE, Henderson IR. 2012. From self-sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10:213–225. [PubMed][CrossRef]
100. Leo JC, Grin I, Linke D. 2012. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos Trans R Soc B Biol Sci 367:1088–1101. [PubMed][CrossRef]
101. Klemm P, Vejborg RM, Sherlock O. 2006. Self-associating autotransporters, SAATs: functional and structural similarities. Int J Med Microbiol 296:187–195. [PubMed][CrossRef]
102. Roux A, Beloin C, Ghigo JM. 2005. Combined inactivation and expression strategy to study gene function under physiological conditions: application to identification of new Escherichia coli adhesins. J Bacteriol 187:1001–1013. [PubMed][CrossRef]
103. Owen P, Meehan M, de Loughry-Doherty H, Henderson I. 1996. Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol Med Microbiol 16:63–76. [PubMed][CrossRef]
104. Hasman H, Chakraborty T, Klemm P. 1999. Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181:4834–4841. [PubMed]
105. Danese PN, Pratt LA, Dove SL, Kolter R. 2000. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol 37:424–432. [PubMed][CrossRef]
106. Grijpstra J, Arenas J, Rutten L, Tommassen J. 2013. Autotransporter secretion: varying on a theme. Res Microbiol 164:562–582. [PubMed][CrossRef]
107. Sherlock O, Schembri MA, Reisner A, Klemm P. 2004. Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J Bacteriol 186:8058–8065. [PubMed][CrossRef]
108. Benz I, Schmidt MA. 2001. Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol Microbiol 40:1403–1413. [PubMed][CrossRef]
109. Sherlock O, Dobrindt U, Jensen JB, Vejborg RM, Klemm P. 2006. Glycosylation of the self-recognizing Escherichia coli Ag43 autotransporter protein. J Bacteriol 188:1798–1807. [PubMed][CrossRef]
110. Lindenthal C, Elsinghorst EA. 1999. Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect Immun 67:4084–4091. [PubMed]
111. Côté J-P, Charbonneau M-È, Mourez M. 2013. Glycosylation of the Escherichia coli TibA self-associating autotransporter influences the conformation and the functionality of the protein. PloS One 8:e80739. doi:10.1371/journal.pone.0080739. [PubMed][CrossRef]
112. Wallecha A, Munster V, Correnti J, Chan T, van der Woude M. 2002. Dam- and OxyR-dependent phase variation of agn43: essential elements and evidence for a new role of DNA methylation. J Bacteriol 184:3338–3347. [PubMed][CrossRef]
113. Chauhan A, Sakamoto C, Ghigo JM, Beloin C. 2013. Did I pick the right colony? Pitfalls in the study of regulation of the phase variable antigen 43 adhesin. PLoS One 8:e73568. doi:10.1371/journal.pone.0073568. [CrossRef]
114. Meng G, Spahich N, Kenjale R, Waksman G, St Geme JW. 2011. Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation. EMBO J 30:3864–3874. [PubMed][CrossRef]
115. Heras B, Totsika M, Peters KM, Paxman JJ, Gee CL, Jarrott RJ, Perugini MA, Whitten AE, Schembri MA. 2014. The antigen 43 structure reveals a molecular Velcro-like mechanism of autotransporter-mediated bacterial clumping. Proc Natl Acad Sci USA 111:457–462. [PubMed][CrossRef]
116. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala’Aldeen D. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68:692–744. [PubMed][CrossRef]
117. Lyskowski A, Leo JC, Goldman A. 2011. Structure and biology of trimeric autotransporter adhesins. Adv Exp Med Biol 715:143–158. [PubMed][CrossRef]
118. El Tahir Y, Skurnik M. 2001. YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol 291:209–218. [PubMed][CrossRef]
119. Heise T, Dersch P. 2006. Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci USA 103:3375–3380. [PubMed][CrossRef]
120. Valle J, Mabbett AN, Ulett GC, Toledo-Arana A, Wecker K, Totsika M, Schembri MA, Ghigo JM, Beloin C. 2008. UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J Bacteriol 190:4147–4161. [PubMed][CrossRef]
121. Raghunathan D, Wells TJ, Morris FC, Shaw RK, Bobat S, Peters SE, Paterson GK, Jensen KT, Leyton DL, Blair JM, Browning DF, Pravin J, Flores-Langarica A, Hitchcock JR, Moraes CT, Piazza RM, Maskell DJ, Webber MA, May RC, MacLennan CA, Piddock LJ, Cunningham AF, Henderson IR. 2011. SadA, a trimeric autotransporter from Salmonella enterica serovar Typhimurium, can promote biofilm formation and provides limited protection against infection. Infect Immun 79:4342–4352. [PubMed][CrossRef]
122. Lazar Adler NR, Dean RE, Saint RJ, Stevens MP, Prior JL, Atkins TP, Galyov EE. 2013. Identification of a predicted trimeric autotransporter adhesin required for biofilm formation of Burkholderia pseudomallei. PLoS One 8:e79461. doi:10.1371/journal.pone.0079461. [CrossRef]
123. Mazar J, Cotter PA. 2007. New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15:508–515. [PubMed][CrossRef]
124. Darsonval A, Darrasse A, Durand K, Bureau C, Cesbron S, Jacques MA. 2009. Adhesion and fitness in the bean phyllosphere and transmission to seed of Xanthomonas fuscans subsp. fuscans. Mol Plant Microbe Interact 22:747–757. [PubMed][CrossRef]
125. Feil H, Feil WS, Lindow SE. 2007. Contribution of fimbrial and afimbrial adhesins of Xylella fastidiosa to attachment to surfaces and virulence to grape. Phytopathology 97:318–324. [PubMed][CrossRef]
126. Ryan RP, Vorholter FJ, Potnis N, Jones JB, Van Sluys MA, Bogdanove AJ, Dow JM. 2011. Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 9:344–355. [PubMed][CrossRef]
127. Webster P, Wu S, Gomez G, Apicella M, Plaut AG, St Geme JW, 3rd. 2006. Distribution of bacterial proteins in biofilms formed by non-typeable Haemophilus influenzae. J Histochem Cytochem 54:829–842. [PubMed][CrossRef]
128. Serra DO, Conover MS, Arnal L, Sloan GP, Rodriguez ME, Yantorno OM, Deora R. 2011. FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS One 6:e28811. doi:10.1371/journal.pone.0028811. [PubMed][CrossRef]
129. Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ, Parsek MR. 2010. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75:827–842. [PubMed][CrossRef]
130. Guo H, Yi W, Song JK, Wang PG. 2008. Current understanding on biosynthesis of microbial polysaccharides. Curr Top Med Chem 8:141–151. [PubMed][CrossRef]
131. Whitney JC, Howell PL. 2013. Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol 21:63–72. [PubMed][CrossRef]
132. Ahimou F, Semmens MJ, Haugstad G, Novak PJ. 2007. Effect of protein, polysaccharide, and oxygen concentration profiles on biofilm cohesiveness. Appl Environ Microbiol 73:2905–2910. [PubMed][CrossRef]
133. Davey ME, O’Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867. [PubMed][CrossRef]
134. Sutherland I. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9. [PubMed]
135. Haag AP. 2006. Mechanical properties of bacterial exopolymeric adhesives and their commercial development, p 1–19. In Smith AM, Callow JA (ed), Biological Adhesives. Springer-Verlag, Berlin. [CrossRef]
136. Korstgens V, Flemming HC, Wingender J, Borchard W. 2001. Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. Water Sci Technol 43:49–57. [PubMed]
137. Franklin MJ, Ohman DE. 1993. Identification of algF in the alginate biosynthetic gene cluster of Pseudomonas aeruginosa which is required for alginate acetylation. J Bacteriol 175:5057–5065. [PubMed]
138. Rinaudo M. 2004. Role of substituents on the properties of some polysaccharides. Biomacromolecules 5:1155–1165. [PubMed][CrossRef]
139. Tielen P, Strathmann M, Jaeger KE, Flemming HC, Wingender J. 2005. Alginate acetylation influences initial surface colonization by mucoid Pseudomonas aeruginosa. Microbiol Res 160:165–176. [PubMed][CrossRef]
140. Villain-Simonnet A, Milas M, Rinaudo M. 2000. A new bacterial polysaccharide (YAS34). I. Characterization of the conformations and conformational transition. Int J Biol Macromol 27:65–75. [PubMed][CrossRef]
141. Wan Z, Brown PJ, Elliott EN, Brun YV. 2013. The adhesive and cohesive properties of a bacterial polysaccharide adhesin are modulated by a deacetylase. Mol Microbiol 88:486–500. [PubMed][CrossRef]
142. Cerca N, Jefferson KK, Maira-Litran T, Pier DB, Kelly-Quintos C, Goldmann DA, Azeredo J, Pier GB. 2007. Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun 75:3406–3413. [PubMed][CrossRef]
143. Itoh Y, Rice JD, Goller C, Pannuri A, Taylor J, Meisner J, Beveridge TJ, Preston JF, 3rd, Romeo T. 2008. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine. J Bacteriol 190:3670–3680. [PubMed][CrossRef]
144. Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, DeLeo FR, Otto M. 2004. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279:54881–54886. [PubMed][CrossRef]
145. Pokrovskaya V, Poloczek J, Little DJ, Griffiths H, Howell PL, Nitz M. 2013. Functional characterization of Staphylococcus epidermidis IcaB, a de-N-acetylase important for biofilm formation. Biochemistry 52:5463–5471. [PubMed][CrossRef]
146. Riley LM, Weadge JT, Baker P, Robinson H, Codee JD, Tipton PA, Ohman DE, Howell PL. 2013. Structural and functional characterization of Pseudomonas aeruginosa AlgX: role of AlgX in alginate acetylation. J Biol Chem 288:22299–22314. [PubMed][CrossRef]
147. Whitney JC, Hay ID, Li C, Eckford PD, Robinson H, Amaya MF, Wood LF, Ohman DE, Bear CE, Rehm BH, Howell PL. 2011. Structural basis for alginate secretion across the bacterial outer membrane. Proc Natl Acad Sci USA 108:13083–13088. [PubMed][CrossRef]
148. Willis LM, Stupak J, Richards MR, Lowary TL, Li J, Whitfield C. 2013. Conserved glycolipid termini in capsular polysaccharides synthesized by ATP-binding cassette transporter-dependent pathways in Gram-negative pathogens. Proc Natl Acad Sci USA 110:7868–7873. [PubMed][CrossRef]
149. Jimenez N, Senchenkova SN, Knirel YA, Pieretti G, Corsaro MM, Aquilini E, Regue M, Merino S, Tomas JM. 2012. Effects of lipopolysaccharide biosynthesis mutations on K1 polysaccharide association with the Escherichia coli cell surface. J Bacteriol 194:3356–3367. [PubMed][CrossRef]
150. Gaastra W, De Graaf FK. 1982. Host-specific fimbrial adhesins of noninvasive enterotoxigenic Escherichia coli strains. Microbiol Rev 46:129. [PubMed]
151. Franco AV, Liu D, Reeves PR. 1996. A Wzz (Cld) protein determines the chain length of K lipopolysaccharide in Escherichia coli O8 and O9 strains. J Bacteriol 178:1903–1907. [PubMed]
152. Jann K, Dengler T, Jann B. 1992. Core-lipid A on the K40 polysaccharide of Escherichia coli O8:K40:H9, a representative of group I capsular polysaccharides. Zentralbl Bakteriol 276:196–204. [CrossRef]
153. Bushell SR, Mainprize IL, Wear MA, Lou H, Whitfield C, Naismith JH. 2013. Wzi is an outer membrane lectin that underpins group 1 capsule assembly in Escherichia coli. Structure 21:844–853. [PubMed][CrossRef]
154. Hardy GG, Allen RC, Toh E, Long M, Brown PJ, Cole-Tobian JL, Brun YV. 2010. A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol Microbiol 76:409–427. [PubMed][CrossRef]
155. Rahn A, Beis K, Naismith JH, Whitfield C. 2003. A novel outer membrane protein, Wzi, is involved in surface assembly of the Escherichia coli K30 group 1 capsule. J Bacteriol 185:5882–5890. [PubMed][CrossRef]
156. Iwashkiw JA, Vozza NF, Kinsella RL, Feldman MF. 2013. Pour some sugar on it: the expanding world of bacterial protein O-linked glycosylation. Mol Microbiol 89:14–28. [PubMed][CrossRef]
157. Song MC, Kim E, Ban YH, Yoo YJ, Kim EJ, Park SR, Pandey RP, Sohng JK, Yoon YJ. 2013. Achievements and impacts of glycosylation reactions involved in natural product biosynthesis in prokaryotes. Appl Microbiol Biotechnol 97:5691–5704. [PubMed][CrossRef]
158. Quintero EJ, Busch K, Weiner RM. 1998. Spatial and temporal deposition of adhesive extracellular polysaccharide capsule and fimbriae by hyphomonas strain MHS-3. Appl Environ Microbiol 64:1246–1255. [PubMed]
159. Ong CJ, Wong ML, Smit J. 1990. Attachment of the adhesive holdfast organelle to the cellular stalk of Caulobacter crescentus. J Bacteriol 172:1448–1456. [PubMed]
160. Smith CS, Hinz A, Bodenmiller D, Larson DE, Brun YV. 2003. Identification of genes required for synthesis of the adhesive holdfast in Caulobacter crescentus. J Bacteriol 185:1432–1442. [PubMed][CrossRef]
161. Poindexter JS. 2006. Dimorphic prosthecate bacteria: the genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron, p 72–90. In Rosenberg E, DeLong EF (ed), The Prokaryotes, vol. 5. Springer, New York. [CrossRef]
162. Poindexter JS. 1964. Biological properties and classification of the Caulobacter group. Bacteriol Rev 28:231–295. [PubMed]
163. Merker RI, Smit J. 1988. Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl Environ Microbiol 54:2078–2085. [PubMed]
164. Fiebig A, Herrou J, Fumeaux C, Radhakrishnan SK, Viollier PH, Crosson S. 2014. A cell cycle and nutritional checkpoint controlling bacterial surface adhesion. PLoS Genet 10:e1004101. doi:10.1371/journal.pgen.1004101. [CrossRef]
165. Toh E, Kurtz HD, Jr, Brun YV. 2008. Characterization of the Caulobacter crescentus holdfast polysaccharide biosynthesis pathway reveals significant redundancy in the initiating glycosyltransferase and polymerase steps. J Bacteriol 190:7219–7231. [PubMed][CrossRef]
166. Li G, Smith CS, Brun YV, Tang JX. 2005. The elastic properties of the Caulobacter crescentus adhesive holdfast are dependent on oligomers of N-acetylglucosamine. J Bacteriol 187:257–265. [PubMed][CrossRef]
167. Tsang PH, Li G, Brun YV, Freund LB, Tang JX. 2006. Adhesion of single bacterial cells in the micronewton range. Proc Natl Acad Sci USA 103:5764–5768. [PubMed][CrossRef]
168. Berne C, Ma X, Licata NA, Neves BR, Setayeshgar S, Brun YV, Dragnea B. 2013. Physiochemical properties of Caulobacter crescentus holdfast: a localized bacterial adhesive. J Phys Chem B 117:10492–10503. [PubMed][CrossRef]
169. Brown PJ, Hardy GG, Trimble MJ, Brun YV. 2008. Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv Microbial Physiol 54:1–101. [PubMed][CrossRef]
170. Rodriguez-Navarro DN, Dardanelli MS, Ruiz-Sainz JE. 2007. Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272:127–136. [PubMed][CrossRef]
171. Laus MC, Logman TJ, Lamers GE, Van Brussel AA, Carlson RW, Kijne JW. 2006. A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. Mol Microbiol 59:1704–1713. [PubMed][CrossRef]
172. Xie F, Williams A, Edwards A, Downie JA. 2012. A plant arabinogalactan-like glycoprotein promotes a novel type of polar surface attachment by Rhizobium leguminosarum. Mol Plant Microbe Interact 25:250–258. [PubMed][CrossRef]
173. Ausmees N, Jacobsson K, Lindberg M. 2001. A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology 147:549–559. [PubMed]
174. Williams A, Wilkinson A, Krehenbrink M, Russo DM, Zorreguieta A, Downie JA. 2008. Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. J Bacteriol 190:4706–4715. [PubMed][CrossRef]
175. Tomlinson AD, Fuqua C. 2009. Mechanisms and regulation of polar surface attachment in Agrobacterium tumefaciens. Curr Opin Microbiol 12:708–714. [PubMed][CrossRef]
176. Loh JT, Ho SC, de Feijter AW, Wang JL, Schindler M. 1993. Carbohydrate binding activities of Bradyrhizobium japonicum: unipolar localization of the lectin BJ38 on the bacterial cell surface. Proc Natl Acad Sci USA 90:3033–3037. [PubMed][CrossRef]
177. Merritt PM, Danhorn T, Fuqua C. 2007. Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189:8005–8014. [PubMed][CrossRef]
178. Xu J, Kim J, Danhorn T, Merritt PM, Fuqua C. 2012. Phosphorus limitation increases attachment in Agrobacterium tumefaciens and reveals a conditional functional redundancy in adhesin biosynthesis. Res Microbiol 163:674–684. [PubMed][CrossRef]
179. Xu J, Kim J, Koestler BJ, Choi JH, Waters CM, Fuqua C. 2013. Genetic analysis of Agrobacterium tumefaciens unipolar polysaccharide production reveals complex integrated control of the motile-to-sessile switch. Mol Microbiol 89:929–948. [PubMed][CrossRef]
180. Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM. 2006. Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 56:195–206. [PubMed][CrossRef]
181. Abdian PL, Caramelo JJ, Ausmees N, Zorreguieta A. 2013. RapA2 is a calcium-binding lectin composed of two highly conserved cadherin-like domains that specifically recognize Rhizobium leguminosarum acidic exopolysaccharides. J Biol Chem 288:2893–2904. [PubMed][CrossRef]
182. Ho SC, Wang JL, Schindler M, Loh JT. 1994. Carbohydrate binding activities of Bradyrhizobium japonicum. III. Lectin expression, bacterial binding, and nodulation efficiency. Plant J 5:873–884. [PubMed][CrossRef]
183. Pérez-Giménez J, Mongiardini EJ, Althabegoiti MJ, Covelli J, Quelas JI, López-García SL, Lodeiro AR. 2009. Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int J Microbiol 2009:719367. [PubMed][CrossRef]
184. Luciano J, Agrebi R, Le Gall AV, Wartel M, Fiegna F, Ducret A, Brochier-Armanet C, Mignot T. 2011. Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet 7:e1002268. doi:10.1371/journal.pgen.1002268. [PubMed][CrossRef]
185. Nan B, Chen J, Neu JC, Berry RM, Oster G, Zusman DR. 2011. Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci USA 108:2498–2503. [PubMed][CrossRef]
186. Nan B, Mauriello EM, Sun IH, Wong A, Zusman DR. 2010. A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol Microbiol 76:1539–1554. [PubMed][CrossRef]
187. Sun M, Wartel M, Cascales E, Shaevitz JW, Mignot T. 2011. Motor-driven intracellular transport powers bacterial gliding motility. Proc Natl Acad Sci USA 108:7559–7564. [PubMed][CrossRef]
188. Zhang Y, Ducret A, Shaevitz J, Mignot T. 2012. From individual cell motility to collective behaviors: insights from a prokaryote, Myxococcus xanthus. FEMS Microbiol Rev 36:149–164. [PubMed][CrossRef]
189. Burchard RP. 1982. Trail following by gliding bacteria. J Bacteriol 152:495–501. [PubMed]
190. Wolgemuth C, Hoiczyk E, Kaiser D, Oster G. 2002. How myxobacteria glide. Curr Biol 12:369–377. [PubMed][CrossRef]
191. Ducret A, Fleuchot B, Bergam P, Mignot T. 2013. Direct live imaging of cell-cell protein transfer by transient outer membrane fusion in Myxococcus xanthus. Elife 2:e00868. doi:10.7554/eLife.00868. [PubMed][CrossRef]
192. Ducret A, Valignat MP, Mouhamar F, Mignot T, Theodoly O. 2012. Wet-surface-enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility. Proc Natl Acad Sci USA 109:10036–10041. [PubMed][CrossRef]
193. Flemming H-C, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol 8:623–633. [PubMed][CrossRef]
194. Stoodley P, Sauer K, Davies D, Costerton JW. 2002. Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209. [PubMed][CrossRef]
195. Wessel AK, Hmelo L, Parsek MR, Whiteley M. 2013. Going local: technologies for exploring bacterial microenvironments. Nat Rev Microbiol 11:337–348. [PubMed][CrossRef]
196. Garnett JA, Martinez-Santos VI, Saldana Z, Pape T, Hawthorne W, Chan J, Simpson PJ, Cota E, Puente JL, Giron JA, Matthews S. 2012. Structural insights into the biogenesis and biofilm formation by the Escherichia coli common pilus. Proc Natl Acad Sci USA 109:3950–3955. [PubMed][CrossRef]
197. Kalivoda EJ, Stella NA, O’Dee DM, Nau GJ, Shanks RM. 2008. The cyclic AMP-dependent catabolite repression system of Serratia marcescens mediates biofilm formation through regulation of type 1 fimbriae. Appl Environ Microbiol 74:3461–3470. [PubMed][CrossRef]
198. Koczan JM, Lenneman BR, McGrath MJ, Sundin GW. 2011. Cell surface attachment structures contribute to biofilm formation and xylem colonization by Erwinia amylovora. Appl Environ Microbiol 77:7031–7039. [PubMed][CrossRef]
199. Mhedbi-Hajri N, Jacques MA, Koebnik R. 2011. Adhesion mechanisms of plant-pathogenic Xanthomonadaceae. Adv Exp Med Biol 715:71–89. [PubMed][CrossRef]
200. Stahlhut SG, Struve C, Krogfelt KA, Reisner A. 2012. Biofilm formation of Klebsiella pneumoniae on urethral catheters requires either type 1 or type 3 fimbriae. FEMS Immunol Med Microbiol 65:350–359. [PubMed][CrossRef]
201. Tomaras AP, Dorsey CW, Edelmann RE, Actis LA. 2003. Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperone-usher pili assembly system. Microbiology 149:3473–3484. [PubMed][CrossRef]
202. Ong CL, Beatson SA, Totsika M, Forestier C, McEwan AG, Schembri MA. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10:183. [PubMed][CrossRef]
203. Di Martino P, Cafferini N, Joly B, Darfeuille-Michaud A. 2003. Klebsiella pneumoniae type 3 pili facilitate adherence and biofilm formation on abiotic surfaces. Res Microbiol 154:9–16. [PubMed][CrossRef]
204. Lappann M, Haagensen JA, Claus H, Vogel U, Molin S. 2006. Meningococcal biofilm formation: structure, development and phenotypes in a standardized continuous flow system. Mol Microbiol 62:1292–1309. [PubMed][CrossRef]
205. Carbonnelle E, Helaine S, Nassif X, Pelicic V. 2006. A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol 61:1510–1522. [PubMed][CrossRef]
206. Marsh JW, Taylor RK. 1999. Genetic and transcriptional analyses of the Vibrio cholerae mannose-sensitive hemagglutinin type 4 pilus gene locus. J Bacteriol 181:1110–1117. [PubMed]
207. Meibom KL, Li XB, Nielsen AT, Wu CY, Roseman S, Schoolnik GK. 2004. The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci USA 101:2524–2529. [PubMed][CrossRef]
208. Moreira CG, Palmer K, Whiteley M, Sircili MP, Trabulsi LR, Castro AF, Sperandio V. 2006. Bundle-forming pili and EspA are involved in biofilm formation by enteropathogenic Escherichia coli. J Bacteriol 188:3952–3961. [PubMed][CrossRef]
209. Bernard CS, Bordi C, Termine E, Filloux A, de Bentzmann S. 2009. Organization and PprB-dependent control of the Pseudomonas aeruginosa tad Locus, involved in Flp pilus biology. J Bacteriol 191:1961–1973. [PubMed][CrossRef]
210. Collinson SK, Clouthier SC, Doran JL, Banser PA, Kay WW. 1996. Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J Bacteriol 178:662–667. [PubMed]
211. Austin JW, Sanders G, Kay WW, Collinson SK. 1998. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol Lett 162:295–301. [PubMed][CrossRef]
212. Dueholm MS, Sondergaard MT, Nilsson M, Christiansen G, Stensballe A, Overgaard MT, Givskov M, Tolker-Nielsen T, Otzen DE, Nielsen PH. 2013. Expression of Fap amyloids in Pseudomonas aeruginosa, P. fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiologyopen 2:365–382. [PubMed][CrossRef]
213. Huber B, Riedel K, Kothe M, Givskov M, Molin S, Eberl L. 2002. Genetic analysis of functions involved in the late stages of biofilm development in Burkholderia cepacia H111. Mol Microbiol 46:411–426. [PubMed][CrossRef]
214. Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, Penades JR, Lasa I. 2005. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58:1322–1339. [PubMed][CrossRef]
215. Loehfelm TW, Luke NR, Campagnari AA. 2008. Identification and characterization of an Acinetobacter baumannii biofilm-associated protein. J Bacteriol 190:1036–1044. [PubMed][CrossRef]
216. Theunissen S, De Smet L, Dansercoer A, Motte B, Coenye T, Van Beeumen JJ, Devreese B, Savvides SN, Vergauwen B. 2010. The 285 kDa Bap/RTX hybrid cell surface protein (SO4317) of Shewanella oneidensis MR-1 is a key mediator of biofilm formation. Res Microbiol 161:144–152. [PubMed][CrossRef]
217. Pérez-Mendoza D, Coulthurst SJ, Humphris S, Campbell E, Welch M, Toth IK, Salmond GP. 2011. A multi-repeat adhesin of the phytopathogen, Pectobacterium atrosepticum, is secreted by a type I pathway and is subject to complex regulation involving a non-canonical diguanylate cyclase. Mol Microbiol 82:719–733. [PubMed][CrossRef]
218. Wu C, Cheng YY, Yin H, Song XN, Li WW, Zhou XX, Zhao LP, Tian LJ, Han JC, Yu HQ. 2013. Oxygen promotes biofilm formation of Shewanella putrefaciens CN32 through a diguanylate cyclase and an adhesin. Sci Rep 3:1945. [PubMed][CrossRef]
219. Hinsa-Leasure SM, Koid C, Tiedje JM, Schultzhaus JN. 2013. Biofilm formation by Psychrobacter arcticus and the role of a large adhesin in attachment to surfaces. Appl Environ Microbiol 79:3967–3973. [PubMed][CrossRef]
220. Torres AG, Perna NT, Burland V, Ruknudin A, Blattner FR, Kaper JB. 2002. Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol Microbiol 45:951–966. [PubMed][CrossRef]
221. Sherlock O, Vejborg RM, Klemm P. 2005. The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect Immun 73:1954–1963. [PubMed][CrossRef]
222. Wells TJ, Sherlock O, Rivas L, Mahajan A, Beatson SA, Torpdahl M, Webb RI, Allsopp LP, Gobius KS, Gally DL, Schembri MA. 2008. EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation. Environ Microbiol 10:589–604. [PubMed][CrossRef]
223. Wells TJ, McNeilly TN, Totsika M, Mahajan A, Gally DL, Schembri MA. 2009. The Escherichia coli O157:H7 EhaB autotransporter protein binds to laminin and collagen I and induces a serum IgA response in O157:H7 challenged cattle. Environ Microbiol 11:1803–1814. [PubMed][CrossRef]
224. Allsopp LP, Totsika M, Tree JJ, Ulett GC, Mabbett AN, Wells TJ, Kobe B, Beatson SA, Schembri MA. 2010. UpaH is a newly identified autotransporter protein that contributes to biofilm formation and bladder colonization by uropathogenic Escherichia coli CFT073. Infect Immun 78:1659–1669. [PubMed][CrossRef]
225. Allsopp LP, Beloin C, Ulett GC, Valle J, Totsika M, Sherlock O, Ghigo JM, Schembri MA. 2012. Molecular characterization of UpaB and UpaC, two new autotransporter proteins of uropathogenic Escherichia coli CFT073. Infect Immun 80:321–332. [PubMed][CrossRef]
226. Zude I, Leimbach A, Dobrindt U. 2013. Prevalence of autotransporters in Escherichia coli: what is the impact of phylogeny and pathotype? Int J Med Microbiol. [Epub ahead of print.] doi:10.1016/j.ijmm.2013.10.006. [PubMed][CrossRef]
227. Kroupitski Y, Brandl MT, Pinto R, Belausov E, Tamir-Ariel D, Burdman S, Sela Saldinger S. 2013. Identification of Salmonella enterica genes with a role in persistence on lettuce leaves during cold storage by recombinase-based in vivo expression technology. Phytopathology 103:362–372. [PubMed][CrossRef]
228. Pearson MM, Laurence CA, Guinn SE, Hansen EJ. 2006. Biofilm formation by Moraxella catarrhalis in vitro: roles of the UspA1 adhesin and the Hag hemagglutinin. Infect Immun 74:1588–1596. [PubMed][CrossRef]
229. Ishikawa M, Nakatani H, Hori K. 2012. AtaA, a new member of the trimeric autotransporter adhesins from Acinetobacter sp. Tol 5 mediating high adhesiveness to various abiotic surfaces. PLoS One 7:e48830. doi:10.1371/journal.pone.0048830. [PubMed][CrossRef]
230. Totsika M, Wells TJ, Beloin C, Valle J, Allsopp LP, King NP, Ghigo JM, Schembri MA. 2012. Molecular characterization of the EhaG and UpaG trimeric autotransporter proteins from pathogenic Escherichia coli. Appl Environ Microbiol 78:2179–2189. [PubMed][CrossRef]
231. Guilhabert MR, Kirkpatrick BC. 2005. Identification of Xylella fastidiosa antivirulence genes: hemagglutinin adhesins contribute a biofilm maturation to X. fastidios and colonization and attenuate virulence. Mol Plant Microbe Interact 18:856–868. [PubMed][CrossRef]
232. Gottig N, Garavaglia BS, Garofalo CG, Orellano EG, Ottado J. 2009. A filamentous hemagglutinin-like protein of Xanthomonas axonopodis pv. citri, the phytopathogen responsible for citrus canker, is involved in bacterial virulence. PLoS One 4:e4358. doi:10.1371/journal.pone.0004358. [CrossRef]
233. Garcia EC, Anderson MS, Hagar JA, Cotter PA. 2013. Burkholderia BcpA mediates biofilm formation independently of interbacterial contact-dependent growth inhibition. Mol Microbiol 89:1213–1225. [PubMed][CrossRef]
234. Evans LR, Linker A. 1973. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bacteriol 116:915–924. [PubMed]
235. Ausmees N, Jonsson H, Hoglund S, Ljunggren H, Lindberg M. 1999. Structural and putative regulatory genes involved in cellulose synthesis in Rhizobium leguminosarum bv. trifolii. Microbiology 145:1253–1262. [PubMed][CrossRef]
236. Matthysse AG, Thomas DL, White AR. 1995. Mechanism of cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177:1076–1081. [PubMed]
237. Matthysse AG, White S, Lightfoot R. 1995. Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177:1069–1075. [PubMed]
238. Ross P, Mayer R, Benziman M. 1991. Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58. [PubMed]
239. Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463. [PubMed][CrossRef]
240. MacRae JD, Smit J. 1991. Characterization of caulobacters isolated from wastewater treatment systems. Appl Environ Microbiol 57:751–758. [PubMed]
241. Moore RL, Marshall KC. 1981. Attachment and rosette formation by hyphomicrobia. Appl Environ Microbiol 42:751–757. [PubMed]
242. Quintero EJ, Weiner RM. 1995. Evidence for the adhesive function of the exopolysaccharide of hyphomonas strain MHS-3 in its attachment to surfaces. Appl Environ Microbiol 61:1897–1903. [PubMed]
243. Yun C, Ely B, Smit J. 1994. Identification of genes affecting production of the adhesive holdfast of a marine caulobacter. J Bacteriol 176:796–803. [PubMed]
244. Wang X, Preston JF, 3rd, Romeo T. 2004. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186:2724–2734. [PubMed][CrossRef]
245. Itoh Y, Wang X, Hinnebusch BJ, Preston JF, 3rd, Romeo T. 2005. Depolymerization of beta-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol 187:382–387. [PubMed][CrossRef]
246. Ghafoor A, Hay ID, Rehm BH. 2011. Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246. [PubMed][CrossRef]
247. Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ. 2004. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186:4466–4475. [PubMed][CrossRef]
248. Byrd MS, Sadovskaya I, Vinogradov E, Lu H, Sprinkle AB, Richardson SH, Ma L, Ralston B, Parsek MR, Anderson EM, Lam JS, Wozniak DJ. 2009. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol Microbiol 73:622–638. [PubMed][CrossRef]
249. Friedman L, Kolter R. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690. [PubMed][CrossRef]
250. Friedman L, Kolter R. 2004. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457–4465. [PubMed][CrossRef]
251. Hufnagel DA, DePas WH, Chapman MR. 2015. The biology of the Escherichia coli extracellular matrix. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms. 2nd ed. ASM Press, Washington, DC, in press. [CrossRef]
252. Wang Y, Haitjema CH, Fuqua C. 2015. The Ctp type IVb pilus locus of Agrobacterium tumefaciens directs formation of the common pili and contributes to reversible surface attachment. J Bacteriol 196:2979–2988. [PubMed][CrossRef]

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During the first step of biofilm formation, initial attachment is dictated by physicochemical and electrostatic interactions between the surface and the bacterial envelope. Depending on the nature of these interactions, attachment can be transient or permanent. To achieve irreversible attachment, bacterial cells have developed a series of surface adhesins promoting specific or nonspecific adhesion under various environmental conditions. This article reviews the recent advances in our understanding of the secretion, assembly, and regulation of the bacterial adhesins during biofilm formation, with a particular emphasis on the fimbrial, nonfimbrial, and discrete polysaccharide adhesins in Gram-negative bacteria.

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Assembly and secretion of fimbrial adhesins. All the assembly pathways are oriented such that the inside of the cell is at the top and the surface to which the adhesin is binding, represented by the thick black line, is at the bottom. The subunits for the three described systems are believed to be transported across the inner membrane by the Sec machinery. (A) A schematic of the CUP pathway represented by the assembly of the type I pilus. FimC (green moon) is a chaperone. FimD (blue-gray) is the outer membrane usher shown as a dimeric channel. FimA (blue bean) is the main pilus subunit. FimF (orange bean) links the tip fibrillum to the main fiber. FimG (yellow bean) is the tip fibrillum. FimH (red bean) is the mannose-specific tip fibrillum adhesin. (B) A schematic of the alternative chaperone-usher pathway using the CS1 pilus as a model. CooB (green moon) is the chaperone. CooC (blue-gray) is the outer membrane usher. CooA (blue bean) is the main pilus subunit. CooD (red circle) is the pilus tip adhesin. (C) Model of curlin assembly as a nucleation-precipitation pathway model. CsgE (green moon) is the chaperone. CsgG (blue-gray) is the outer membrane usher. CsgA (blue beans) is the main curlin subunit. CsgB (dark blue bean) is the minor curlin subunit. CsgF (red bean) is the outer membrane protein needed for curlin polymerization and CsgB localization. CsgC (red ball) may be important for CsgG localization. Abbreviations: IM, inner membrane; CW, cell wall; OM, outer membrane.

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Type IV assembly and secretion pathway. Given that the type IV pili have similar elements, we are using the type IVa pilus as the model for biogenesis. Many type IVa proteins utilize the Sec machinery to translocate the inner membrane (aqua pore). PilA (blue sphere) is the main pilus subunit. FimU, PilE, PilX, PilW, and PilV are minor pilins (red, yellow, light blue, green, and purple spheres, respectively). The prepilins are processed by PilD (orange integral IM protein), the prepilin protease. PilB (red bean) is the ATPase that supplies energy for pilus assembly, and PilU/PilT (purple bean) is the ATPase for pilus retraction. PilC (green porin) is an inner membrane protein of the motor complex for assembly of the pilus. PilM, PilN, PilO, PilP, and FimV are the alignment complex. PilQ is the multimeric secretin in the outer membane that translocates the pilus outside the cell. PilF is a pilotin needed for localization of the PilQ in the OM. FimV is a peptidoglycan binding protein needed for multimerization of PilQ. Abbreviations: IM, inner membrane; CW, cell wall; OM, outer membrane.

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Schematic overview of the various secretion systems of nonfimbrial adhesins. The type 1 secretion system (T1SS) and three classes of type 5 secretion system (T5SS) (onomeric utotransporter dhesins [MAA], rimeric utotransporter dhesins [TAA], and two-partner secretion [TPS] systems) are represented. In T1SS, the adhesin is exported directly from the cytoplasm to the extracellular milieu via a pore comprised of three proteins. In T5SS, the adhesin is translocated from the cytoplasm to the periplasm by the Sec machinery and auto-assembled in the outer membrane. See text for more details. Abbreviations: IM, inner membrane; CW, cell wall; OM, outer membrane.

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Nonfimbrial adhesin organization. See text for details. Green, signal sequence for proper localization and processing; turquoise, core domain; orange, glycine-rich repeated domain (brackets depict the variable number of repeats); magenta, serine-rich C-terminal region; navy blue, passenger domain; red, translocator domain.

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Polysaccharide biosynthesis pathways. Overview of the Wzx/Wzy-, ABC-transporter-, and synthase-dependent exopolysaccharide biosynthesis pathways. Only the key components for each pathway are indicated on the diagram. In the Wzx/Wzy-dependent pathway, the polysaccharide repeat unit assembly is initiated on an undecaprenyl phosphate acceptor moiety located in the inner leaflet of the inner membrane, which is then transported across the inner membrane by the flippase, Wzx. The polymerization into high–molecular weight polysaccharide occurs in the periplasm by the action of the polymerase Wzy. The export and secretion of the polysaccharide through the outer membrane are facilitated by the uter membrane olysaccharide eport (OPX) and the olysaccharide oolymerase (PCP) protein families. Depending on the polysaccharide being synthesized, the nascent polymer could be anchored to the outer membrane via a specific protein, such as Wzi. In the ABC transporter–dependent pathway, the entire polysaccharide chain is assembled into the cytoplasm on a lipid acceptor that is then transported across the inner membrane by the ABC transporter. As observed for the Wzx/Wzy-dependant pathway, the export and secretion of the polysaccharide through the outer membrane also involve the OPX and PCP protein families. In the synthase-dependent pathway, both the polymerization and the transport of the polymer across the inner membrane are carried out by the same membrane-embedded glycosyl transferase. The export and secretion of the polysaccharide through the outer membrane are facilitated by a molecular chaperone and a β-barrel porin. Abbreviations: IM, inner membrane; CW, cell wall; OM, outer membrane.

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Selected examples of discrete polysaccharides. AF488-conjugated wheat germ agglutinin lectin labelling of the holdfast in (A) , (B) (courtesy of Chao Jiang), (C) (courtesy of Chao Jiang), and (D) (courtesy of Ellen Quardokus). (E) AF488-conjugated wheat germ agglutinin lectin labelling of the UPP in . (F) FITC-conjugated ConA lectin labelling of the slime in .

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Examples of fimbrial adhesins involved in biofilm formation

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Type IV pilus components

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Selected examples of nonfimbrial adhesins experimentally shown to be involved in biofilm formation by Gram-negative bacteria

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015
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Selected examples of aggregative polysaccharides experimentally shown to be involved in biofilm formation by Gram-negative bacteria

Source: microbiolspec July 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0018-2015

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