The University of Southampton
University of Southampton Institutional Repository

The SpoIIQ-SpoIIIAH complex of Clostridium difficile controls forespore engulfment and late stages of gene expression and spore morphogenesis

The SpoIIQ-SpoIIIAH complex of Clostridium difficile controls forespore engulfment and late stages of gene expression and spore morphogenesis
The SpoIIQ-SpoIIIAH complex of Clostridium difficile controls forespore engulfment and late stages of gene expression and spore morphogenesis

Engulfment of the forespore by the mother cell is a universal feature of endosporulation. In Bacillus subtilis, the forespore protein SpoIIQ and the mother cell protein SpoIIIAH form a channel, essential for endosporulation, through which the developing spore is nurtured. The two proteins also form a backup system for engulfment. Unlike in B. subtilis, SpoIIQ of Clostridium difficile has intact LytM zinc-binding motifs. We show that spoIIQ or spoIIIAH deletion mutants of C. difficile result in anomalous engulfment, and that disruption of the SpoIIQ LytM domain via a single amino acid substitution (H120S) impairs engulfment differently. SpoIIQ and SpoIIQ(H120S) interact with SpoIIIAH throughout engulfment. SpoIIQ, but not SpoIIQ(H120S) , binds Zn(2+) , and metal absence alters the SpoIIQ-SpoIIIAH complex in vitro. Possibly, SpoIIQ(H120S) supports normal engulfment in some cells but not a second function of the complex, required following engulfment completion. We show that cells of the spoIIQ or spoIIIAH mutants that complete engulfment are impaired in post-engulfment, forespore and mother cell-specific gene expression, suggesting a channel-like function. Both engulfment and a channel-like function may be ancestral functions of SpoIIQ-SpoIIIAH while the requirement for engulfment was alleviated through the emergence of redundant mechanisms in B. subtilis and related organisms.

Amino Acid Sequence, Amino Acid Substitution, Bacterial Proteins/chemistry, Clostridioides difficile/physiology, Gene Expression Regulation, Bacterial, Protein Binding, Protein Interaction Domains and Motifs, Sequence Deletion, Spores, Bacterial
0950-382X
204-28
Serrano, Mónica
131f2fee-4325-486b-aeee-6a9be8c00ed6
Crawshaw, Adam D
c3daa995-52e5-487b-a379-0638f43525fb
Dembek, Marcin
0d86d0a0-9d80-451c-b479-4849ddfda137
Monteiro, João M
7c46a82d-ce0f-4c47-ba99-334e2e1a326e
Pereira, Fátima C
a9396948-26f9-4f13-8f83-a22fec1dd0e0
Pinho, Mariana Gomes
f66fb68d-82c7-4fb4-b34b-7e65ef780476
Fairweather, Neil F
82f5d88f-35bc-490f-a1db-ddd7e115e4d6
Salgado, Paula S
84389463-dd34-464d-8db2-f5452037886f
Henriques, Adriano O
eb4668e6-bfb0-4df3-bf8e-93dbd1cc5b2d
Serrano, Mónica
131f2fee-4325-486b-aeee-6a9be8c00ed6
Crawshaw, Adam D
c3daa995-52e5-487b-a379-0638f43525fb
Dembek, Marcin
0d86d0a0-9d80-451c-b479-4849ddfda137
Monteiro, João M
7c46a82d-ce0f-4c47-ba99-334e2e1a326e
Pereira, Fátima C
a9396948-26f9-4f13-8f83-a22fec1dd0e0
Pinho, Mariana Gomes
f66fb68d-82c7-4fb4-b34b-7e65ef780476
Fairweather, Neil F
82f5d88f-35bc-490f-a1db-ddd7e115e4d6
Salgado, Paula S
84389463-dd34-464d-8db2-f5452037886f
Henriques, Adriano O
eb4668e6-bfb0-4df3-bf8e-93dbd1cc5b2d

Serrano, Mónica, Crawshaw, Adam D, Dembek, Marcin, Monteiro, João M, Pereira, Fátima C, Pinho, Mariana Gomes, Fairweather, Neil F, Salgado, Paula S and Henriques, Adriano O (2016) The SpoIIQ-SpoIIIAH complex of Clostridium difficile controls forespore engulfment and late stages of gene expression and spore morphogenesis. Molecular Microbiology, 100 (1), 204-28. (doi:10.1111/mmi.13311).

Record type: Article

Abstract

Engulfment of the forespore by the mother cell is a universal feature of endosporulation. In Bacillus subtilis, the forespore protein SpoIIQ and the mother cell protein SpoIIIAH form a channel, essential for endosporulation, through which the developing spore is nurtured. The two proteins also form a backup system for engulfment. Unlike in B. subtilis, SpoIIQ of Clostridium difficile has intact LytM zinc-binding motifs. We show that spoIIQ or spoIIIAH deletion mutants of C. difficile result in anomalous engulfment, and that disruption of the SpoIIQ LytM domain via a single amino acid substitution (H120S) impairs engulfment differently. SpoIIQ and SpoIIQ(H120S) interact with SpoIIIAH throughout engulfment. SpoIIQ, but not SpoIIQ(H120S) , binds Zn(2+) , and metal absence alters the SpoIIQ-SpoIIIAH complex in vitro. Possibly, SpoIIQ(H120S) supports normal engulfment in some cells but not a second function of the complex, required following engulfment completion. We show that cells of the spoIIQ or spoIIIAH mutants that complete engulfment are impaired in post-engulfment, forespore and mother cell-specific gene expression, suggesting a channel-like function. Both engulfment and a channel-like function may be ancestral functions of SpoIIQ-SpoIIIAH while the requirement for engulfment was alleviated through the emergence of redundant mechanisms in B. subtilis and related organisms.

This record has no associated files available for download.

More information

Published date: 1 April 2016
Additional Information: © 2015 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Keywords: Amino Acid Sequence, Amino Acid Substitution, Bacterial Proteins/chemistry, Clostridioides difficile/physiology, Gene Expression Regulation, Bacterial, Protein Binding, Protein Interaction Domains and Motifs, Sequence Deletion, Spores, Bacterial

Identifiers

Local EPrints ID: 470700
URI: http://eprints.soton.ac.uk/id/eprint/470700
ISSN: 0950-382X
PURE UUID: 961ecea3-15e0-45de-a4c5-ff9a615761cd
ORCID for Fátima C Pereira: ORCID iD orcid.org/0000-0002-1288-6481

Catalogue record

Date deposited: 18 Oct 2022 16:42
Last modified: 17 Mar 2024 04:14

Export record

Altmetrics

Contributors

Author: Mónica Serrano
Author: Adam D Crawshaw
Author: Marcin Dembek
Author: João M Monteiro
Author: Fátima C Pereira ORCID iD
Author: Mariana Gomes Pinho
Author: Neil F Fairweather
Author: Paula S Salgado
Author: Adriano O Henriques

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×