Abstract
To interact with the external environments, bacteria often display long proteinaceous appendages on their cell surface, called pili or fimbriae. These non-flagellar thread-like structures are polymers composed of covalently or non-covalently interacting repeated pilin subunits. Distinct pilus classes can be identified on basis of their assembly pathways, including chaperone-usher pili, type V pili, type IV pili, curli and fap fibers, conjugative and type IV secretion pili, as well as sortase-mediated pili. Pili play versatile roles in bacterial physiology, and can be involved in adhesion and host cell invasion, DNA and protein secretion and uptake, biofilm formation, cell motility and more. Recent advances in structure determination of components involved in the various pilus systems has enabled a better molecular understanding of their mechanisms of assembly and function. In this chapter we describe the diversity in structure, biogenesis and function of the different pilus systems found in Gram-positive and Gram-negative bacteria, and review their potential as anti-microbial targets.
Magdalena Lukaszczyk, Brajabandhu Pradhan—Authors contributed equally.
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This work was supported by VIB and the ERC under consolidator grant BAS-SBBT.
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Addendum on e-pili
Addendum on e-pili
Geobacter species such as Geobacter sulfurreducens possess micrometer long conductive filaments or “nanowires” that mediate extracellular electron transport (Reguera et al. 2005), and play a role in respiration (Malvankar et al. 2011) and interspecific electron exchange (Summers et al. 2010). Nanowire-expressing bacteria are associated with many important redox processes such as carbon and mineral recycling in soil, metal corrosion, conversion of organic waste to methane and electricity (Malvankar and Lovley 2014). The molecular nature of these nanowires has been obscure, however, and for a long time they were considered to be composed of Type IV pilus-like PilA subunits (Childers et al. 2002), with the conductive properties proposed to be coming from stacked aromatic residues in the pilus subunits, or through association with the C-type cytochrome OmcS (Leang et al. 2013).
The recent cryoEM structures of isolated conductive pili or “e-pili” from G. sulfurreducens have now revealed their unique structure, composition and electron transport mechanism (Filman et al. 2018; Wang et al. 2019). This study shows Geobacter e-pili are composed of a unique noncovalent linear polymer of the cytochrome OmcS (Fig. 12.6). OmcS was previously known to be essential for bacterial growth on insoluble electron acceptors such as Fe (III) oxide and electrodes, but had not been directly implicated as the main nanowire component (Holmes et al. 2006; Mehta et al. 2005). The structures show each OmcS subunit contains six stacked hemes that are placed within 3.5–6 Å to each other in a trajectory that spans the length of the nanowire and results in electric coupling within and across subunits. The hemes are found in parallel pairs, each pair oriented perpendicular to the next. In the parallel arrangement, the hemes are present within a range of 3.4–4.1 Å while in the perpendicular arrangement they are within a range of 5.4–6.1 Å (Fig. 12.6). The parallel arrangement is expected to maximize electron coupling while the perpendicular arrangement is thought to enhance the structural stability of the subunit. For each heme group, two histidines situated axially form coordination bonds with the iron atom present at the center, and the vinyl groups form covalent thioester bonds with cysteine. In the filament, subunits associate in a head-to-tail arrangement, with each subunit in contact with only one preceding and succeeding subunit, through an inter-subunit contact comprising ~2,600 Å2 surface area. Histidine 16 of each subunit coordinates an adjacent heme group present in the succeeding subunit. These inter-subunit coordination bonds are proposed to maximize the structural stability of the nanowire. This cross-interface heme coordination is speculated to result from a domain swapping of the C-terminal helix, a process that has been observed in induced cytochrome polymerization (Hirota et al. 2010; Wang et al. 2019). Little is known about the secretion and in vivo assembly pathway of OmcS e-pili. Although it is now evident that PilA is not the main structural subunit of the nanowires, previous genetic studies clearly associate it with the presence of Geobacter’s e-pili and the secretion of OmcS to the extracellular space (Liu et al. 2018; Richter et al. 2012). Deletion or mutation of PilA leads to the absence of OmcS on the surface (Reguera et al. 2005) while overexpression of PilA leads to overproduction of nanowires (Leang et al. 2013; Summers et al. 2010). The cryoEM structures now clearly demonstrate PilA is not found as a component of e-pili (Filman et al. 2018; Wang et al. 2019). Whether PilA is found as an additional extracellular fiber or acts as a pseudopilus of a T2SS, and where and how OmcS subunits polymerize and associate with the cell surface will require further study.
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Lukaszczyk, M., Pradhan, B., Remaut, H. (2019). The Biosynthesis and Structures of Bacterial Pili. In: Kuhn, A. (eds) Bacterial Cell Walls and Membranes . Subcellular Biochemistry, vol 92. Springer, Cham. https://doi.org/10.1007/978-3-030-18768-2_12
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