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Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins

Quorum sensing (QS) is a unique mechanism for microorganisms to coordinate their activities through intercellular communication, including four main types of autoinducer-1 (AI-1, namely, N-acyl homoserine lactone [AHL]), AI-2, AI-3, and diffusible signaling factor [DSF]) based on signaling molecules...

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Autores principales: Huang, Shanshan, Liu, Xueduan, Yang, Weiyi, Ma, Liyuan, Li, Huiying, Liu, Rui, Qiu, Jingxuan, Li, Yiran
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9040811/
https://www.ncbi.nlm.nih.gov/pubmed/35400206
http://dx.doi.org/10.1128/msystems.01491-21
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author Huang, Shanshan
Liu, Xueduan
Yang, Weiyi
Ma, Liyuan
Li, Huiying
Liu, Rui
Qiu, Jingxuan
Li, Yiran
author_facet Huang, Shanshan
Liu, Xueduan
Yang, Weiyi
Ma, Liyuan
Li, Huiying
Liu, Rui
Qiu, Jingxuan
Li, Yiran
author_sort Huang, Shanshan
collection PubMed
description Quorum sensing (QS) is a unique mechanism for microorganisms to coordinate their activities through intercellular communication, including four main types of autoinducer-1 (AI-1, namely, N-acyl homoserine lactone [AHL]), AI-2, AI-3, and diffusible signaling factor [DSF]) based on signaling molecules. Quorum quenching (QQ) enzymes can disrupt the QS phenomenon by inactivating signaling molecules. QS is proposed to regulate biofilm formation in extremely acidic environments, but the QS/QQ-related genomic features in most acidophilic bacteria are still largely unknown. Here, genome annotation of 83 acidophiles from the genera Acidithiobacillus, Leptospirillum, Sulfobacillus, and Acidiphilium altogether revealed the existence of AI-1, AI-3, DSF, and AhlD (AHL degradation enzyme). The conservative investigation indicated that some QS/QQ-related proteins harbored key residues or motifs, which were necessary for their activities. Phylogenetic analysis showed that LuxI/R (AI-1 synthase/receptor), QseE/F (two-component system of AI-3), and RpfC/G (two-component system of DSF) exhibited similar evolutionary patterns within each pair. Meanwhile, proteins clustered approximately according to the species taxonomy. The widespread Acidithiobacillus strains, especially A. ferrooxidans, processed AI-1, AI-3, and DSF systems as well as the AhlD enzyme, which were favorable for their mutual information exchange and collective regulation of gene expression. Some members of the Sulfobacillus and Acidiphilium without AHL production capacity contained the AhlD enzyme, which may evolve for niche competition, while DSF in Leptospirillum and Acidithiobacillus could potentially combine with the cyclic diguanylate (c-di-GMP) pathway for self-defense and niche protection. This work will shed light on our understanding of the extent of communication networks and adaptive evolution among acidophiles via QS/QQ coping with environmental changes. IMPORTANCE Understanding cell-cell communication QS is highly relevant for comprehending the regulatory and adaptive mechanisms among acidophiles in extremely acidic ecosystems. Previous studies focused on the existence and functionality of a single QS system in several acidophilic strains. Four representative genera were selected to decipher the distribution and role of QS and QQ integrated with the conservative and evolutionary analysis of related proteins. It was implicated that intra- or intersignaling circuits may work effectively based on different QS types to modulate biofilm formation and energy metabolism among acidophilic microbes. Some individuals could synthesize QQ enzymes for specific QS molecular inactivation to inhibit undesirable acidophile species. This study expanded our knowledge of the fundamental cognition and biological roles underlying the dynamical communication interactions among the coevolving acidophiles and provided a novel perspective for revealing their environmental adaptability.
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spelling pubmed-90408112022-04-27 Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins Huang, Shanshan Liu, Xueduan Yang, Weiyi Ma, Liyuan Li, Huiying Liu, Rui Qiu, Jingxuan Li, Yiran mSystems Research Article Quorum sensing (QS) is a unique mechanism for microorganisms to coordinate their activities through intercellular communication, including four main types of autoinducer-1 (AI-1, namely, N-acyl homoserine lactone [AHL]), AI-2, AI-3, and diffusible signaling factor [DSF]) based on signaling molecules. Quorum quenching (QQ) enzymes can disrupt the QS phenomenon by inactivating signaling molecules. QS is proposed to regulate biofilm formation in extremely acidic environments, but the QS/QQ-related genomic features in most acidophilic bacteria are still largely unknown. Here, genome annotation of 83 acidophiles from the genera Acidithiobacillus, Leptospirillum, Sulfobacillus, and Acidiphilium altogether revealed the existence of AI-1, AI-3, DSF, and AhlD (AHL degradation enzyme). The conservative investigation indicated that some QS/QQ-related proteins harbored key residues or motifs, which were necessary for their activities. Phylogenetic analysis showed that LuxI/R (AI-1 synthase/receptor), QseE/F (two-component system of AI-3), and RpfC/G (two-component system of DSF) exhibited similar evolutionary patterns within each pair. Meanwhile, proteins clustered approximately according to the species taxonomy. The widespread Acidithiobacillus strains, especially A. ferrooxidans, processed AI-1, AI-3, and DSF systems as well as the AhlD enzyme, which were favorable for their mutual information exchange and collective regulation of gene expression. Some members of the Sulfobacillus and Acidiphilium without AHL production capacity contained the AhlD enzyme, which may evolve for niche competition, while DSF in Leptospirillum and Acidithiobacillus could potentially combine with the cyclic diguanylate (c-di-GMP) pathway for self-defense and niche protection. This work will shed light on our understanding of the extent of communication networks and adaptive evolution among acidophiles via QS/QQ coping with environmental changes. IMPORTANCE Understanding cell-cell communication QS is highly relevant for comprehending the regulatory and adaptive mechanisms among acidophiles in extremely acidic ecosystems. Previous studies focused on the existence and functionality of a single QS system in several acidophilic strains. Four representative genera were selected to decipher the distribution and role of QS and QQ integrated with the conservative and evolutionary analysis of related proteins. It was implicated that intra- or intersignaling circuits may work effectively based on different QS types to modulate biofilm formation and energy metabolism among acidophilic microbes. Some individuals could synthesize QQ enzymes for specific QS molecular inactivation to inhibit undesirable acidophile species. This study expanded our knowledge of the fundamental cognition and biological roles underlying the dynamical communication interactions among the coevolving acidophiles and provided a novel perspective for revealing their environmental adaptability. American Society for Microbiology 2022-04-11 /pmc/articles/PMC9040811/ /pubmed/35400206 http://dx.doi.org/10.1128/msystems.01491-21 Text en Copyright © 2022 Huang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Huang, Shanshan
Liu, Xueduan
Yang, Weiyi
Ma, Liyuan
Li, Huiying
Liu, Rui
Qiu, Jingxuan
Li, Yiran
Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins
title Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins
title_full Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins
title_fullStr Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins
title_full_unstemmed Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins
title_short Insights into Adaptive Mechanisms of Extreme Acidophiles Based on Quorum Sensing/Quenching-Related Proteins
title_sort insights into adaptive mechanisms of extreme acidophiles based on quorum sensing/quenching-related proteins
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9040811/
https://www.ncbi.nlm.nih.gov/pubmed/35400206
http://dx.doi.org/10.1128/msystems.01491-21
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