Cellulose in Bacterial Biofilms

  • Diego O. Serra
  • Regine HenggeEmail author
Part of the Biologically-Inspired Systems book series (BISY, volume 12)


Many bacteria produce cellulose as an exopolysaccharide component of the extracellular matrix in biofilms, which are large aggregates of bacterial cells often attached to abiotic or biotic surfaces. Cellulose has been particularly well studied in two model bacteria, Komagataeibacter xylinus and Escherichia coli. The widely conserved bacterial cellulose synthase consists of a membrane-inserted core complex, whose BcsA subunit provides for a glucosyltransferase activity that is allosterically activated by the second messenger c-di-GMP and which, together with the BcsB subunit, forms a transmembrane channel for co-synthetic secretion of cellulose. Various accessory Bcs proteins further conduct cellulose to the cell surface, where glucan chains are aligned and assembled into higher order fibrils. The corresponding genes are generally organized in operons that are easily detected in genome sequences. K. xylinus produces highly crystalline cellulose, which alone or in technically generated composite materials is now widely used in food and paper technology or in medical applications. A surprise in the bacterial cellulose field was the recent discovery that E. coli and many other bacteria “decorate” their cellulose with a phospholipid-derived phosphoethanolamine (pEtN) group in a post-synthetic process catalyzed by BcsG at the outer side of the cytoplasmic membrane. This enzymatic process not only represents the first natural chemical modification of cellulose but enables pEtN-cellulose to form nanocomposites with amyloid fibers in the extracellular matrix of biofilms. The result is tissue-like cohesion and elasticity, which allow growing macrocolony or pellicle biofilms to buckle up and fold into macroscopic morphological patterns of wrinkles and high ridges. These recent discoveries hold promise that other types of modified cellulose with novel chemical and biomechanical properties are yet be found in nature or could even be generated by synthetic biology approaches.



Research in the Hengge lab mentioned in this review has been funded by the Deutsche Forschungsgemeinschaft (DFG grants He1556/17-1, He1556/20-1, and He1556/21-1 to RH), the European Research Council under the European Union’s Seventh Framework Programme (ERC-AdG 249780 to R.H.), and the Alexander von Humboldt Foundation (postdoctoral fellowship to DOS).


  1. Aas FE, Egge-Jacobsen W, Winther-Larsen HC, Lovold C, Hitchen PG, Dell A, Koomey M (2006) Neisseria gonorrhoeae type IV pili undergo multisite, hierarchical modifications with phosphoethanolamine and phosphocholine requiring an enzyme structurally related to lipopolysaccharide phosphoethanolamine transferases. J Biol Chem 281:27712–27723PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ahmad I, Lamprokostopoulou A, Le Guyon S, Streck E, Barthel M, Peters V et al (2011) Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS One 6:e28351PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ahmad I, Rouf SF, Sun L, Cimdins A, Shafeeq S, Le Guyon S et al (2016) BcsZ inhibits biofilm phenotypes and promotes virulence by blocking cellulose production in Salmonella enterica serovar Typhimurium. Microb Cell Factories 15:177. Scholar
  4. Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3–6PubMedCrossRefPubMedCentralGoogle Scholar
  5. Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285PubMedCrossRefGoogle Scholar
  6. Augimeri RV, Varley AJ, Strap JL (2015) Establishing a role for bacterial cellulose in environmental interactions: lessons learned from diverse biofilm-producing Proteobacteria. Front Microbiol 6:1282. Scholar
  7. Bassis CM, Visick KL (2010) The cyclic-di-GMP phosphodiesterase BinA negatively regulates cellulose-containing biofilms in Vibrio fischeri. J Bacteriol 192:1269–1278PubMedPubMedCentralCrossRefGoogle Scholar
  8. Beloin C, Roux A, Ghigo JM (2008) Escherichia coli biofilms. Curr Top Microbiol Immunol 322:249–289PubMedPubMedCentralGoogle Scholar
  9. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98:11621–11626PubMedCrossRefPubMedCentralGoogle Scholar
  10. Brett CT (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161–199PubMedCrossRefGoogle Scholar
  11. Brown AJ (1886) XLIII.—on an acetic ferment which forms cellulose. J Chem Soc Trans 49:432–439CrossRefGoogle Scholar
  12. Brown RM Jr, Willison JH, Richardson CL (1976) Cellulose biosynthesis in Acetobacter xylinum: visualization of the site of synthesis and direct measurement of the in vivo process. Proc Natl Acad Sci USA 73:4565–4569PubMedCrossRefPubMedCentralGoogle Scholar
  13. Brown PK, Dozois CM, Nickerson CA, Zuppardo A, Terlonge J, Curtiss R 3rd (2001) MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41:349–363PubMedCrossRefPubMedCentralGoogle Scholar
  14. Buckminster Fuller R (1961) Tensegrity. Portfolio Art News Annu 4:112–127Google Scholar
  15. Bureau TE, Brown RM (1987) In vitro synthesis of cellulose II from a cytoplasmic membrane fraction of Acetobacter xylinum. Proc Natl Acad Sci USA 84:6985–6989PubMedCrossRefPubMedCentralGoogle Scholar
  16. Cerca N, Jefferson KK (2008) Effect of growth conditions on poly-N-acetylglucosamine expression and biofilm formation in Escherichia coli. FEMS Microbiol Lett 283:36–41PubMedCrossRefPubMedCentralGoogle Scholar
  17. Chang AL, Tuckerman JR, Gonzalez G, Mayer R, Weinhouse H, Volman G et al (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40:3420–3426PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M et al (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855PubMedPubMedCentralCrossRefGoogle Scholar
  19. Christen M, Christen B, Folcher M, Schauerte A, Jenal U (2005) Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280:30829–30837PubMedCrossRefPubMedCentralGoogle Scholar
  20. Cohn F (1877) Untersuchungen über Bacterien. IV Beiträge zur Biologie der Bacillen Beiträge zur biologie der Pflanzen 7:249–276Google Scholar
  21. Cullen TW, Madsen JA, Ivanov PL, Brodbelt JS, Trent MS (2012) Characterization of unique modification of flagellar rod protein FlgG by Campylobacter jejuni lipid A phosphoethanolamine transferase, linking bacterial locomotion and antimicrobial peptide resistance. J Biol Chem 287:3326–3336PubMedCrossRefPubMedCentralGoogle Scholar
  22. Da Re S, Ghigo JM (2006) A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J Bacteriol 188:3073–3087PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dragos A, Kovacs AT (2017) The peculiar functions of the bacterial extracellular matrix. Trends Microbiol 25:257–266PubMedCrossRefPubMedCentralGoogle Scholar
  24. Fang X, Ahmad I, Blanka A, Schottkowski M, Cimdins A, Galperin MY et al (2014) GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol Microbiol 93:439–452PubMedPubMedCentralCrossRefGoogle Scholar
  25. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633PubMedCrossRefPubMedCentralGoogle Scholar
  26. Franklin MJ, Nivens DE, Weadge JT, Howell PL (2011) Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front Microbiol 2:167. Scholar
  27. Friedman L, Kolter R (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457–4465PubMedPubMedCentralCrossRefGoogle Scholar
  28. Garcia B, Latasa C, Solano C, Garcia-del Portillo F, Gamazo C, Lasa I (2004) Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54:264–277PubMedCrossRefPubMedCentralGoogle Scholar
  29. Guhados G, Wan W, Hutter JL (2005) Measurement of the elastic modulus of single bacterial cellulose fibers using atomic force microscopy. Langmuir 21:6642–6646PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hackney JM, Atalla RH, Vander Hart DL (1994) Modification of crystallinity and crystalline structure of Acetobacter xylinum cellulose in the presence of water-soluble beta-1,4-linked polysaccharides: 13C-NMR evidence. Int J Biol Macromol 16:215–218PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hammerschmidt S, Wolff S, Hocke A, Rosseau S, Muller E, Rohde M (2005) Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun 73:4653–4667PubMedPubMedCentralCrossRefGoogle Scholar
  32. Harding NE, Cleary JM, Cabanas DK, Rosen IG, Kang KS (1987) Genetic and physical analyses of a cluster of genes essential for xanthan gum biosynthesis in Xanthomonas campestris. J Bacteriol 169:2854–2861PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hengge R (2016) Trigger phosphodiesterases as a novel class of c-di-GMP effector proteins. Philos Trans R Soc Lond Ser B Biol Sci 371. Scholar
  34. Hollenbeck EC, Antonoplis A, Chai C, Thongsomboon W, Fuller GG, Cegelski L (2018) Phosphoethanolamine cellulose enhances curli-mediated adhesion of uropathogenic Escherichia coli to bladder epithelial cells. Proc Natl Acad Sci USA 115:10106–10111PubMedCrossRefPubMedCentralGoogle Scholar
  35. Hu SQ, Gao YG, Tajima K, Sunagawa N, Zhou Y, Kawano S et al (2010) Structure of bacterial cellulose synthase subunit D octamer with four inner passageways. Proc Natl Acad Sci USA 107:17957–17961PubMedCrossRefPubMedCentralGoogle Scholar
  36. Hung C, Zhou Y, Pinkner JS, Dodson KW, Crowley JR, Heuser J et al (2013) Escherichia coli biofilms have an organized and complex extracellular matrix structure. MBio 4:e00645–e00613. Scholar
  37. Ingber DE (2008) Tensegrity-based mechanosensing from macro to micro. Prog Biophys Mol Biol 97:163–179PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jenal U, Reinders A, Lori C (2017) Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol 15:271–284PubMedCrossRefPubMedCentralGoogle Scholar
  39. Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS, Sadovskaya I et al (2015) Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proc Natl Acad Sci USA 112:11353–11358PubMedCrossRefPubMedCentralGoogle Scholar
  40. Jonas R, Farah LF (1998) Production and application of microbial cellulose. Polym Degrad Stab 59:101–106CrossRefGoogle Scholar
  41. Kimura S, Chen HP, Saxena IM, Brown RM Jr, Itoh T (2001) Localization of c-di-GMP-binding protein with the linear terminal complexes of Acetobacter xylinum. J Bacteriol 183:5668–5674PubMedPubMedCentralCrossRefGoogle Scholar
  42. Klauck G, Serra DO, Possling A, Hengge R (2018) Spatial organization of different sigma factor activities and c-di-GMP signalling within the three-dimensional landscape of a bacterial biofilm. Open Biol 8. Scholar
  43. Kolpak FJ, Blackwell J (1976) Determination of the structure of cellulose II. Macromolecules 9:273–278PubMedCrossRefPubMedCentralGoogle Scholar
  44. Krasteva PV, Giglio KM, Sondermann H (2012) Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci 21:929–948PubMedPubMedCentralCrossRefGoogle Scholar
  45. Krasteva PV, Bernal-Bayard J, Travier L, Martin FA, Kaminski PA, Karimova G et al (2017) Insights into the structure and assembly of a bacterial cellulose secretion system. Nat Commun 8:2065. Scholar
  46. Larsson PT, Wickholm K, Iversen T (1997) A CP/MAS13C NMR investigation of molecular ordering in celluloses. Carbohydr Res 302:19–25CrossRefGoogle Scholar
  47. Le Quéré B, Ghigo JM (2009) BcsQ is an essential component of the Escherichia coli cellulose biosynthesis apparatus that localizes at the bacterial cell pole. Mol Microbiol 72:724–740PubMedCrossRefPubMedCentralGoogle Scholar
  48. Lin FC, Brown RM Jr, Drake RR Jr, Haley BE (1990) Identification of the uridine 5’-diphosphoglucose (UDP-Glc) binding subunit of cellulose synthase in Acetobacter xylinum using the photoaffinity probe 5-azido-UDP-Glc. J Biol Chem 265:4782–4784PubMedPubMedCentralGoogle Scholar
  49. Lindenberg S, Klauck G, Pesavento C, Klauck E, Hengge R (2013) The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. EMBO J 32:2001–2014PubMedPubMedCentralCrossRefGoogle Scholar
  50. Matthysse AG, Marry M, Krall L, Kaye M, Ramey BE, Fuqua C, White AR (2005) The effect of cellulose overproduction on binding and biofilm formation on roots by Agrobacterium tumefaciens. Mol Plant-Microbe Interact 18:1002–1010PubMedCrossRefPubMedCentralGoogle Scholar
  51. Matthysse AG, Deora R, Mishra M, Torres AG (2008) Polysaccharides cellulose, poly-beta-1,6-n-acetyl-D-glucosamine, and colanic acid are required for optimal binding of Escherichia coli O157:H7 strains to alfalfa sprouts and K-12 strains to plastic but not for binding to epithelial cells. Appl Environ Microbiol 74:2384–2390PubMedPubMedCentralCrossRefGoogle Scholar
  52. Mazeau K (2015) The hygroscopic power of amorphous cellulose: a modeling study. Carbohydr Polym 117:585–591PubMedCrossRefPubMedCentralGoogle Scholar
  53. Mazur O, Zimmer J (2011) Apo- and cellopentaose-bound structures of the bacterial cellulose synthase subunit BcsZ. J Biol Chem 286:17601–17606PubMedPubMedCentralCrossRefGoogle Scholar
  54. McManus JB, Deng Y, Nagachar N, Kao TH, Tien M (2016) AcsA-AcsB: the core of the cellulose synthase complex from Gluconacetobacter hansenii ATCC23769. Enzym Microb Technol 82:58–65CrossRefGoogle Scholar
  55. Mehta K, Pfeffer S, Malcolm Brown RJ (2015) Characterization of an acsD disruption mutant provides additional evidence for the hierarchical cell-directed self-assembly of cellulose in Gluconacetobacter xylinus. Cellulose 22:119–137CrossRefGoogle Scholar
  56. Morgan JL, Strumillo J, Zimmer J (2013) Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–186PubMedCrossRefPubMedCentralGoogle Scholar
  57. Morgan JL, McNamara JT, Zimmer J (2014) Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nat Struct Mol Biol 21:489–496PubMedPubMedCentralCrossRefGoogle Scholar
  58. Nakai T, Nishiyama Y, Kuga S, Sugano Y, Shoda M (2002) ORF2 gene involves in the construction of high-order structure of bacterial cellulose. Biochem Biophys Res Commun 295:458–462PubMedCrossRefPubMedCentralGoogle Scholar
  59. Nobles DR, Romanovicz DK, Brown RM Jr (2001) Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? Plant Physiol 127:529–542PubMedPubMedCentralCrossRefGoogle Scholar
  60. Omadjela O, Narahari A, Strumillo J, Melida H, Mazur O, Bulone V, Zimmer J (2013) BcsA and BcsB form the catalytically active core of bacterial cellulose synthase sufficient for in vitro cellulose synthesis. Proc Natl Acad Sci USA 110:17856–17861PubMedCrossRefPubMedCentralGoogle Scholar
  61. Pang J, Liu X, Yang J, Lu F, Wang B, Xu F et al (2016) Synthesis of highly polymerized water-soluble cellulose acetate by the side reaction in carboxylate ionic liquid 1-ethyl-3-methylimidazolium acetate. Sci Rep 6:33725. Scholar
  62. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, Giese B, Jenal U (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18:715–727PubMedPubMedCentralCrossRefGoogle Scholar
  63. Pontes MH, Lee EJ, Choi J, Groisman EA (2015) Salmonella promotes virulence by repressing cellulose production. Proc Natl Acad Sci USA 112:5183–5188PubMedCrossRefPubMedCentralGoogle Scholar
  64. Povolotsky TL, Hengge R (2016) Genome-based comparison of cyclic di-GMP signaling in pathogenic and commensal Escherichia coli strains. J Bacteriol 198:111–126PubMedCrossRefPubMedCentralGoogle Scholar
  65. Pritt B, O’Brien L, Winn W (2007) Mucoid Pseudomonas in cystic fibrosis. Am J Clin Pathol 128:32–34PubMedCrossRefPubMedCentralGoogle Scholar
  66. Pultz IS, Christen M, Kulasekara HD, Kennard A, Kulasekara B, Miller SI (2012) The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86:1424–1440PubMedPubMedCentralCrossRefGoogle Scholar
  67. Qi Y, Rao F, Luo Z, Liang ZX (2009) A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 48:10275–10285PubMedCrossRefPubMedCentralGoogle Scholar
  68. Rajwade JM, Paknikar KM, Kumbhar JV (2015) Applications of bacterial cellulose and its composites in biomedicine. Appl Microbiol Biotechnol 99:2491–2511PubMedCrossRefPubMedCentralGoogle Scholar
  69. Rao EV, Ramana KS (1991) Structural studies of a polysaccharide isolated from the green seaweed Chaetomorpha anteninna. Carbohydr Res 217:163–170PubMedCrossRefPubMedCentralGoogle Scholar
  70. Richter AM, Povolotsky TL, Wieler LH, Hengge R (2014) Cyclic-di-GMP signalling and biofilm-related properties of the Shiga toxin-producing 2011 German outbreak Escherichia coli O104:H4. EMBO Mol Med 6:1622–1637PubMedPubMedCentralCrossRefGoogle Scholar
  71. Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107:2230–2234PubMedCrossRefPubMedCentralGoogle Scholar
  72. Römling U (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62:1234–1246PubMedCrossRefPubMedCentralGoogle Scholar
  73. Römling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–557PubMedPubMedCentralCrossRefGoogle Scholar
  74. Römling U, Rohde M, Olsen A, Normark S, Reinkoster J (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36:10–23PubMedCrossRefPubMedCentralGoogle Scholar
  75. Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R et al (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281PubMedCrossRefPubMedCentralGoogle Scholar
  77. Ross P, Mayer R, Benziman M (1991) Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58PubMedPubMedCentralGoogle Scholar
  78. Sarenko O, Klauck G, Wilke FM, Pfiffer V, Richter AM, Herbst S et al (2017) More than enzymes that make or break cyclic di-GMP-local signaling in the interactome of GGDEF/EAL domain proteins of Escherichia coli. MBio 8.
  79. Saxena IM, Kudlicka K, Okuda K, Brown RM Jr (1994) Characterization of genes in the cellulose-synthesizing operon (acs operon) of Acetobacter xylinum: implications for cellulose crystallization. J Bacteriol 176:5735–5752PubMedPubMedCentralCrossRefGoogle Scholar
  80. Schirmer T (2016) C-di-GMP synthesis: structural aspects of evolution, catalysis and regulation. J Mol Biol 428:3683–3701PubMedCrossRefPubMedCentralGoogle Scholar
  81. Schmidt AJ, Ryjenkov DA, Gomelsky M (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187:4774–4781PubMedPubMedCentralCrossRefGoogle Scholar
  82. Serra DO, Hengge R (2014) Stress responses go three dimensional – the spatial order of physiological differentiation in bacterial macrocolony biofilms. Environ Microbiol 16:1455–1471PubMedPubMedCentralCrossRefGoogle Scholar
  83. Serra DO, Hengge R (2017) Experimental detection and visualization of the extracellular matrix in macrocolony biofilms. Methods Mol Biol 1657:133–145PubMedCrossRefPubMedCentralGoogle Scholar
  84. Serra DO, Richter AM, Hengge R (2013a) Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol 195:5540–5554PubMedPubMedCentralCrossRefGoogle Scholar
  85. Serra DO, Richter AM, Klauck G, Mika F, Hengge R (2013b) Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. MBio 4:e00103–e00113. Scholar
  86. Serra DO, Klauck G, Hengge R (2015) Vertical stratification of matrix production is essential for physical integrity and architecture of macrocolony biofilms of Escherichia coli. Environ Microbiol 17:5073–5088PubMedPubMedCentralCrossRefGoogle Scholar
  87. Shaw RK, Lasa I, Garcia BM, Pallen MJ, Hinton JC, Berger CN, Frankel G (2011) Cellulose mediates attachment of Salmonella enterica serovar Typhimurium to tomatoes. Environ Microbiol Rep 3:569–573PubMedCrossRefPubMedCentralGoogle Scholar
  88. Shibazaki H, Saito M, Kuga S, Okano T (1998) Native cellulose II production by Acetobacter xylinum under physical constraints. Cellulose 5:165–173CrossRefGoogle Scholar
  89. Shon AS, Bajwa RP, Russo TA (2013) Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: a new and dangerous breed. Virulence 4:107–118PubMedPubMedCentralCrossRefGoogle Scholar
  90. Simm R, Morr M, Kader A, Nimtz M, Römling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134PubMedCrossRefPubMedCentralGoogle Scholar
  91. Singletary LA, Karlinsey JE, Libby SJ, Mooney JP, Lokken KL, Tsolis RM et al (2016) Loss of Multicellular Behavior in Epidemic African Nontyphoidal Salmonella enterica Serovar Typhimurium ST313 Strain D23580. MBio 7:e02265. Scholar
  92. Smit G, Kijne JW, Lugtenberg BJ (1987) Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol 169:4294–4301PubMedPubMedCentralCrossRefGoogle Scholar
  93. Solano C, Garcia B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I (2002) Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43:793–808PubMedCrossRefPubMedCentralGoogle Scholar
  94. Sommerfeldt N, Possling A, Becker G, Pesavento C, Tschowri N, Hengge R (2009) Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155:1318–1331PubMedCrossRefPubMedCentralGoogle Scholar
  95. Stanisławska A (2016) Bacterial nanocellulose as a microbiological derived nanomaterial. Adv Mater Sci 16:45–57CrossRefGoogle Scholar
  96. Sun L, Vella P, Schnell R, Polyakova A, Bourenkov G, Li F et al (2018) Structural and functional characterization of the BcsG subunit of the cellulose synthase in Salmonella typhimurium. J Mol Biol 430:3170–3189PubMedCrossRefPubMedCentralGoogle Scholar
  97. Sunagawa N, Fujiwara T, Yoda T, Kawano S, Satoh Y, Yao M et al (2013) Cellulose complementing factor (Ccp) is a new member of the cellulose synthase complex (terminal complex) in Acetobacter xylinum. J Biosci Bioeng 115:607–612PubMedCrossRefPubMedCentralGoogle Scholar
  98. Sutherland IW (1970) Structural studies on colanic acid, the common exopolysaccharide found in the Enterobacteriaceae, by partial acid hydrolysis. Biochem J 115:935–945CrossRefGoogle Scholar
  99. Tahara N, Tonouchi N, Yano H, Yoshinaga F (1998) Purification and Characterization of Exo-1,4-b-Glucosidase from Acetobacter xylinum BPR2001. J Ferment Bioeng 85:589–594CrossRefGoogle Scholar
  100. Tal R, Wong HC, Calhoon R, Gelfand D, Fear AL, Volman G et al (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180:4416–4425PubMedPubMedCentralGoogle Scholar
  101. Thongsomboon W, Serra DO, Possling A, Hadjineophytou C, Hengge R, Cegelski L (2018) Phosphoethanolamine cellulose: a naturally produced chemically modified cellulose. Science 359:334–338PubMedCrossRefPubMedCentralGoogle Scholar
  102. Tonouchi N, Tahara N, Kojima Y, Nakai T, Sakai F, Hayashi T et al (1997) A beta-glucosidase gene downstream of the cellulose synthase operon in cellulose-producing Acetobacter. Biosci Biotechnol Biochem 61:1789–1790PubMedCrossRefPubMedCentralGoogle Scholar
  103. Toyosaki H, Naritomi T, Seto A, Matsuoka M, Tsuchida T, Yoshinaga F (1995) Screening of bacterial cellulose-producing Acetobacter strains suitable for agitated culture. Biosci Biotech Biochem 59:1498–1502CrossRefGoogle Scholar
  104. Visick KL, Quirke KP, McEwen SM (2013) Arabinose induces pellicle formation by Vibrio fischeri. Appl Environ Microbiol 79:2069–2080PubMedPubMedCentralCrossRefGoogle Scholar
  105. Vitta S, Thiruvengadam V (2012) Multifunctional bacterial cellulose and nanoparticle-embedded composites. Curr Sci 102:1398–1405Google Scholar
  106. Wang X, Rochon M, Lamprokostopoulou A, Lunsdorf H, Nimtz M, Römling U (2006) Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell Mol Life Sci 63:2352–2363PubMedCrossRefPubMedCentralGoogle Scholar
  107. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R (2006) Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 62:1014–1034PubMedCrossRefPubMedCentralGoogle Scholar
  108. Whitney JC, Howell PL (2013) Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol 21:63–72PubMedCrossRefPubMedCentralGoogle Scholar
  109. Williams WS, Cannon RE (1989) Alternative environmental roles for cellulose produced by Acetobacter xylinum. Appl Environ Microbiol 55:2448–2452PubMedPubMedCentralGoogle Scholar
  110. Wong HC, Fear AL, Calhoon RD, Eichinger GH, Mayer R, Amikam D et al (1990) Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc Natl Acad Sci USA 87:8130–8134PubMedCrossRefPubMedCentralGoogle Scholar
  111. Yamanaka S, Watanabe K, Kitamura N, Iguchi M, Mitsuhashi S, Nishi Y, Uryu M (1989) The structure and mechanical properties of sheets prepared from bacterial cellulose. J Mater Sci 24:3141–3145CrossRefGoogle Scholar
  112. Yan J, Nadell CD, Stone HA, Wingreen NS, Bassler BL (2017) Extracellular-matrix-mediated osmotic pressure drives Vibrio cholerae biofilm expansion and cheater exclusion. Nat Commun 8:327. Scholar
  113. Yang L, Hengzhuang W, Wu H, Damkiaer S, Jochumsen N, Song Z et al (2012) Polysaccharides serve as scaffold of biofilms formed by mucoid Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 65:366–376PubMedCrossRefPubMedCentralGoogle Scholar
  114. Yaron S, Römling U (2014) Biofilm formation by enteric pathogens and its role in plant colonization and persistence. Microb Biotechnol 7:496–516PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yildiz FH, Schoolnik GK (1999) Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci USA 96:4028–4033PubMedCrossRefPubMedCentralGoogle Scholar
  116. Yip ES, Grublesky BT, Hussa EA, Visick KL (2005) A novel, conserved cluster of genes promotes symbiotic colonization and sigma-dependent biofilm formation by Vibrio fischeri. Mol Microbiol 57:1485–1498PubMedCrossRefPubMedCentralGoogle Scholar
  117. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463PubMedCrossRefPubMedCentralGoogle Scholar
  118. Zogaj X, Bokranz W, Nimtz M, Römling U (2003) Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect Immun 71:4151–4158PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Humboldt-Universität zu Berlin, Institut für Biologie, MikrobiologieBerlinGermany

Personalised recommendations