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Chapter 9 : Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria

Authors: Cécile Berne1, Adrien Ducret2, Gail G. Hardy3, Yves V. Brun4
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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
Content Type: Monograph
Publication Year: 2015

Category: Environmental Microbiology

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Abstract:

The ability of bacterial cells to adhere to and interact with surfaces to eventually form a biofilm is a crucial trait for the survival of any microorganism in a complex environment. As a result, different strategies aimed at providing specific or nonspecific interactions between the bacterial cell and the surface have evolved. While adhesion to abiotic surfaces is usually mediated by nonspecific interactions, adhesion to biotic surfaces typically requires a specific receptor-ligand interaction ( ). In both cases, these interactions usually originate from the same fundamental physicochemical forces: covalent bonds, Van der Waals forces, electrostatic forces, and acid-base interactions ( ). Strong adhesion occurs if a bacterium and a surface are capable of forming either covalent, ionic, or metallic bonds, but weaker forces, such as polar, hydrogen bonding, or Van der Waals interactions, can also strengthen or achieve strong interactions when a high number of contacts are involved ( ). Due the net negative charge of their cell envelopes, bacteria are subjected to repulsive electrostatic forces when approaching surfaces. Bacterial cells also encounter repulsive hydrodynamic forces near the surface in a liquid environment. To overcome these two repulsive barriers, bacteria typically use organelles, such as flagella or pili, which act either as an active propeller or a grappling hook ( ). Once on the surface, the cell can enhance attachment to the surface via specific and/or nonspecific adhesins to eventually trigger irreversible attachment. This irreversible attachment is strongly influenced by environmental factors (i.e., pH, salinity, etc.) and the physicochemical properties of the surface (i.e., rugosity, hydrophobicity, charge, etc.) but also by the presence of the conditioning film, a layer of organic and inorganic contaminants adsorbed on the surface which changes its physicochemical properties ( ). To achieve permanent adhesion under such variable conditions, bacterial cells have developed a series of adhesins able to facilitate adhesion under various environmental conditions ( ). In this article, we will focus exclusively on nonspecific adhesins, which are primarily responsible for biofilm formation and bacterial adhesion to abiotic surfaces. We will review the current knowledge of fimbrial, nonfimbrial, and discrete polysaccharide adhesins involved in adhesion to abiotic surfaces and cell aggregation 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, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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Adhesins Involved in Attachment to Abiotic Surfaces by 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, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
/content/10.1128/9781555817466.chap9.fig9-1
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 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.
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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 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.

Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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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 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 2

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.

Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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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) (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.
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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) (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.

Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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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 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.

Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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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 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.
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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 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.

Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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Figure 6
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 .
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Figure 6

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 .

Citation: Berne C, Ducret A, Hardy G, Brun Y. 2015. Adhesins Involved in Attachment to Abiotic Surfaces by Gram-Negative Bacteria, p 163-199. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0018-2015
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