Global biochemical and structural analysis of the type IV pilus from the Gram-positive bacterium<i>Streptococcus sanguinis</i>

Berry, Jamie-Lee; Gurung, Ishwori; Anonsen, Jan Haug; Spielman, Ingrid; Harper, Elliot; Hall, A.; Goosens, Vivianne J.; Raynaud, Claire; Koomey, Michael; Biais, Nicolas; Matthews, Steve; Pelicic, Vladimir

doi:10.1101/459388

Cited by 2 publications

(7 citation statements)

References 57 publications

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“…These structures point to a hypothetical evolutionary scenario during which truncation of the antiparallel β-sheet in a canonical type IV pilin might have led to a purely helical ComGC protostructure. Intriguingly, this scenario "works" particularly well with PilE1, a major subunit of S. sanguinis T4P, which has two short α-helices in the loop connecting α1 and the antiparallel β-sheet (11).…”

Section: Discussionmentioning

confidence: 96%

“…DNA is subsequently bound by the DNA receptor ComEA and further translocated across the CM through the ComEC channel (9). In diderm competent species, the T4F involved in DNA uptake is a subtype of T4P, known as T4aP (11), which rapid depolymerisation is powered by the retraction ATPase PilT (IPR006321), generating exceptionally large tensile forces (12). In brief, T4aP bind DNA directly, via one of their major or minor (low abundance) pilin subunits (13), and then are retracted by PilT, bringing DNA to the ComEA receptor (14).…”

Section: Introductionmentioning

confidence: 99%

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The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold

Sheppard

Berry

Denise

et al. 2020

Journal of Biological Chemistry

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Type IV filaments (T4F), which are helical assemblies of type IV pilins, constitute a superfamily of filamentous nanomachines virtually ubiquitous in prokaryotes that mediate a wide variety of functions. The competence (Com) pilus is a widespread T4F, mediating DNA uptake (the first step in natural transformation) in bacteria with one membrane (monoderms), an important mechanism of horizontal gene transfer. Here, we report the results of genomic, phylogenetic, and structural analyses of ComGC, the major pilin subunit of Com pili. By performing a global comparative analysis, we show that Com pili genes are virtually ubiquitous in Bacilli, a major monoderm class of Firmicutes. This also revealed that ComGC displays extensive sequence conservation, defining a monophyletic group among type IV pilins. We further report ComGC solution structures from two naturally competent human pathogens, Streptococcus sanguinis (ComGCSS) and Streptococcus pneumoniae (ComGCSP), revealing that this pilin displays extensive structural conservation. Strikingly, ComGCSS and ComGCSP exhibit a novel type IV pilin fold that is purely helical. Results from homology modeling analyses suggest that the unusual structure of ComGC is compatible with helical filament assembly. Because ComGC displays such a widespread distribution, these results have implications for hundreds of monoderm species.

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold

Sheppard

Berry

Denise

et al. 2020

Journal of Biological Chemistry

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“…B) and 3D structure (Fig. C) (Berry et al , ). It remains to be seen whether such a heteropolymeric structure might be a more general property of Tfp in monoderms, which awaits purification and biochemical characterisation of filaments in other species.…”

Section: Monoderm Bacteria Produce Tfpmentioning

confidence: 98%

“…S. sanguinis Tfp, which have a Tfp morphology (Fig. A), were purified to homogeneity and shown to be heteropolymers of two similar pilins (PilE1 and PilE2) in a 4:3 ratio (Berry et al , ). These pilins exhibit canonical class III signal peptide (Fig.…”

Section: Monoderm Bacteria Produce Tfpmentioning

confidence: 99%

“…As in diderms, filament retraction is powered by the retraction of ATPase PilT, which is dispensable for piliation (Gurung et al , ). It is important to underline that the term ‘minor pilin’ is just generic, only indicating that the corresponding proteins are cleaved by the prepilin peptidase to become low abundance components of the filaments (Berry et al , ). This does not imply that these proteins play identical or even similar functions in each system, which is supported by the fact that minor pilins in different systems share no sequence homology.…”

Section: Tfp Biogenesis Machineries In Monoderm Bacteria: the Beauty mentioning

confidence: 99%

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Monoderm bacteria: the new frontier for type IV pilus biology

Pelicic

2019

Molecular Microbiology

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Summary In the diverse world of bacterial pili, type IV pili (Tfp) are unique for two reasons: their multifunctionality and ubiquity. This latter feature offers an extraordinary possibility, that is, to perform comparative studies in evolutionarily distant species in order to improve our fragmentary understanding of Tfp biology. Regrettably, such potential has remained largely untapped, because, for 20 years, Tfp have only been characterised in diderm bacteria. However, recent studies of Tfp in monoderms have started closing the gap, revealing many interesting commonalities and a few significant differences, extending the frontiers of knowledge of Tfp biology. Here, I review the current state of the art of the Tfp field in monoderm bacteria and discuss resulting implications for our general understanding of the assembly and function of these widespread filamentous nanomachines.

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Global biochemical and structural analysis of the type IV pilus from the Gram-positive bacteriumStreptococcus sanguinis

Abstract: Type IV pili (Tfp)

Cited by 2 publications

References 57 publications

The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold

The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold

Monoderm bacteria: the new frontier for type IV pilus biology

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