Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria
- Authors: Cécile Berne1, Adrien Ducret2, Gail G. Hardy3, Yves V. Brun4
- Editors: Mahmoud Ghannoum5, Matthew Parsek6, Marvin Whiteley7, Pranab Mukherjee8
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VIEW AFFILIATIONS HIDE AFFILIATIONSAffiliations: 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
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Received 20 February 2015 Accepted 03 March 2015 Published 24 July 2015
- Correspondence: 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.
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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.




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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.

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Figures

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FIGURE 1
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 E. coli 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 E. coli 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 E. coli 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.

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FIGURE 2
Type IV assembly and secretion pathway. Given that the type IV pili have similar elements, we are using the P. aeruginosa 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.

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FIGURE 3
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) (monomeric autotransporter adhesins [MAA], trimeric autotransporter adhesins [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.

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FIGURE 4
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.

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FIGURE 5
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 outer membrane polysaccharide export (OPX) and the polysaccharide copolymerase (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.

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FIGURE 6
Selected examples of discrete polysaccharides. AF488-conjugated wheat germ agglutinin lectin labelling of the holdfast in (A) C. crescentus, (B) A. biprosthecum (courtesy of Chao Jiang), (C) Asticcacaulis excentricus (courtesy of Chao Jiang), and (D) Hyphomicrobium vulgare (courtesy of Ellen Quardokus). (E) AF488-conjugated wheat germ agglutinin lectin labelling of the UPP in A. tumefaciens. (F) FITC-conjugated ConA lectin labelling of the slime in M. xanthus.
Tables

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TABLE 1
Examples of fimbrial adhesins involved in biofilm formation

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TABLE 2
Type IV pilus components

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TABLE 3
Selected examples of nonfimbrial adhesins experimentally shown to be involved in biofilm formation by Gram-negative bacteria

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TABLE 4
Selected examples of aggregative polysaccharides experimentally shown to be involved in biofilm formation by Gram-negative bacteria
Supplemental Material
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