Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling

Abstract The collective behavior of bacteria is regulated by quorum sensing (QS). Autoinducer-2 (AI-2) is a common QS signal that regulates the behavior of both Gram-positive and Gram-negative bacteria. Despite the plethora of processes described to be influenced by AI-2 in diverse Gram-negative bac...

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Main Authors: Qin Xiong, Huihui Zhang, Xia Shu, Xiting Sun, Haichao Feng, Zhihui Xu, Ákos T. Kovács, Ruifu Zhang, Yunpeng Liu
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:npj Biofilms and Microbiomes
Online Access:https://doi.org/10.1038/s41522-024-00594-6
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author Qin Xiong
Huihui Zhang
Xia Shu
Xiting Sun
Haichao Feng
Zhihui Xu
Ákos T. Kovács
Ruifu Zhang
Yunpeng Liu
author_facet Qin Xiong
Huihui Zhang
Xia Shu
Xiting Sun
Haichao Feng
Zhihui Xu
Ákos T. Kovács
Ruifu Zhang
Yunpeng Liu
author_sort Qin Xiong
collection DOAJ
description Abstract The collective behavior of bacteria is regulated by quorum sensing (QS). Autoinducer-2 (AI-2) is a common QS signal that regulates the behavior of both Gram-positive and Gram-negative bacteria. Despite the plethora of processes described to be influenced by AI-2 in diverse Gram-negative bacteria, the AI-2-regulated processes in Bacilli are relatively unexplored. Here, we describe a novel function for AI-2 in Bacillus velezensis SQR9 related to the sporulation. AI-2 inhibited the initiation of sporulation through the phosphatase RapC and the DNA binding regulator ComA. Using biochemistry experiments, we demonstrated that AI-2 interacts with RapC to stimulate its binding to ComA, which leads to an inactive ComA and subsequently a sporulation inhibition. The AI-2 molecule could be shared across species for inhibiting Bacillus sporulation and it also plays the same role in different soil conditions. Our study revealed a novel function and regulatory mechanism of AI-2 in inhibiting sporulation in Bacilli.
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institution OA Journals
issn 2055-5008
language English
publishDate 2024-11-01
publisher Nature Portfolio
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series npj Biofilms and Microbiomes
spelling doaj-art-eeacbbcfd1f74f7f90feed835672d0072025-08-20T02:18:15ZengNature Portfolionpj Biofilms and Microbiomes2055-50082024-11-0110111110.1038/s41522-024-00594-6Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signalingQin Xiong0Huihui Zhang1Xia Shu2Xiting Sun3Haichao Feng4Zhihui Xu5Ákos T. Kovács6Ruifu Zhang7Yunpeng Liu8National Engineering Research Center of Navel Orange, Gannan Normal UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityState Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, the Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesState Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, the Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesJiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityJiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural UniversityFaculty of Science - Institute of Biology, Leiden University, Sylviusweg 73State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, the Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesState Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, the Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural SciencesAbstract The collective behavior of bacteria is regulated by quorum sensing (QS). Autoinducer-2 (AI-2) is a common QS signal that regulates the behavior of both Gram-positive and Gram-negative bacteria. Despite the plethora of processes described to be influenced by AI-2 in diverse Gram-negative bacteria, the AI-2-regulated processes in Bacilli are relatively unexplored. Here, we describe a novel function for AI-2 in Bacillus velezensis SQR9 related to the sporulation. AI-2 inhibited the initiation of sporulation through the phosphatase RapC and the DNA binding regulator ComA. Using biochemistry experiments, we demonstrated that AI-2 interacts with RapC to stimulate its binding to ComA, which leads to an inactive ComA and subsequently a sporulation inhibition. The AI-2 molecule could be shared across species for inhibiting Bacillus sporulation and it also plays the same role in different soil conditions. Our study revealed a novel function and regulatory mechanism of AI-2 in inhibiting sporulation in Bacilli.https://doi.org/10.1038/s41522-024-00594-6
spellingShingle Qin Xiong
Huihui Zhang
Xia Shu
Xiting Sun
Haichao Feng
Zhihui Xu
Ákos T. Kovács
Ruifu Zhang
Yunpeng Liu
Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling
npj Biofilms and Microbiomes
title Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling
title_full Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling
title_fullStr Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling
title_full_unstemmed Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling
title_short Autoinducer-2 relieves soil stress-induced dormancy of Bacillus velezensis by modulating sporulation signaling
title_sort autoinducer 2 relieves soil stress induced dormancy of bacillus velezensis by modulating sporulation signaling
url https://doi.org/10.1038/s41522-024-00594-6
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