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Monoderm bacteria: the new frontier for type IV pilus biology.

ABSTRACT: 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.

SUBMITTER: Pelicic V

PROVIDER: S-EPMC6916266 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Monoderm bacteria: the new frontier for type IV pilus biology.

Pelicic Vladimir V

Molecular microbiology 20191008 6

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 monoderm ...[more]

PMID: 31556183

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Project description:UnlabelledType IV pili (T4Ps) are surface appendages used by Gram-negative and Gram-positive pathogens for motility and attachment to epithelial surfaces. In Gram-negative bacteria, such as the important pediatric pathogen enteropathogenic Escherichia coli (EPEC), during extension and retraction, the pilus passes through an outer membrane (OM) pore formed by the multimeric secretin complex. The secretin is common to Gram-negative assemblies, including the related type 2 secretion (T2S) system and the type 3 secretion (T3S) system. The N termini of the secretin monomers are periplasmic and in some systems have been shown to mediate substrate specificity. In this study, we mapped the topology of BfpB, the T4P secretin from EPEC, using a combination of biochemical and biophysical techniques that allowed selective identification of periplasmic and extracellular residues. We applied rules based on solved atomic structures of outer membrane proteins (OMPs) to generate our topology model, combining the experimental results with secondary structure prediction algorithms and direct inspection of the primary sequence. Surprisingly, the C terminus of BfpB is extracellular, a result confirmed by flow cytometry for BfpB and a distantly related T4P secretin, PilQ, from Pseudomonas aeruginosa. Keeping with prior evidence, the C termini of two T2S secretins and one T3S secretin were not detected on the extracellular surface. On the basis of our data and structural constraints, we propose that BfpB forms a beta barrel with 16 transmembrane beta strands. We propose that the T4P secretins have a C-terminal segment that passes through the center of each monomer.ImportanceSecretins are multimeric proteins that allow the passage of secreted toxins and surface structures through the outer membranes (OMs) of Gram-negative bacteria. To date, there have been no atomic structures of the C-terminal region of a secretin, although electron microscopy (EM) structures of the complex are available. This work provides a detailed topology prediction of the membrane-spanning domain of a type IV pilus (T4P) secretin. Our study used innovative techniques to provide new and comprehensive information on secretin topology, highlighting similarities and differences among secretin subfamilies. Additionally, the techniques used in this study may prove useful for the study of other OM proteins.

Dataset Information

Monoderm bacteria: the new frontier for type IV pilus biology.

Publications

Monoderm bacteria: the new frontier for type IV pilus biology.

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