Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria

Quorum Sensing (QS) is a well-studied intercellular communication mechanism in bacteria, regulating collective behaviors such as biofilm formation, virulence, and antibiotic resistance. However, cell–cell signaling in haloarchaea remains largely unexplored. The coexistence of bacteria and archaea in...

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Main Authors: Thomas P. Thompson, Alessandro Busetti, Brendan F. Gilmore
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/11/5/1271
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author Thomas P. Thompson
Alessandro Busetti
Brendan F. Gilmore
author_facet Thomas P. Thompson
Alessandro Busetti
Brendan F. Gilmore
author_sort Thomas P. Thompson
collection DOAJ
description Quorum Sensing (QS) is a well-studied intercellular communication mechanism in bacteria, regulating collective behaviors such as biofilm formation, virulence, and antibiotic resistance. However, cell–cell signaling in haloarchaea remains largely unexplored. The coexistence of bacteria and archaea in various environments, coupled with the known cell–cell signaling mechanisms in both prokaryotic and eukaryotic microorganisms and the presence of cell–cell signaling mechanisms in both prokaryotic and eukaryotic microorganisms, suggests a possibility for haloarchaea to possess analogous cell–cell signaling or QS systems. Recently, N-acylhomoserine lactone (AHL)-like compounds were identified in haloarchaea; yet, their precise role—for example, persister cell formation—remains ambiguous. This study investigated the capacity of crude supernatant extract from the haloarchaeon <i>Halorubrum saccharovorum</i> CSM52 to stimulate bacterial AHL-dependent QS phenotypes using bioreporter strains. Our findings reveal that these crude extracts induced several AHL-dependent bioreporters and modulated pyocyanin and pyoverdine production in <i>Pseudomonas aeruginosa</i>. Importantly, our study suggests cross-domain communication between archaea and bacterial pathogens, providing evidence for archaea potentially influencing bacterial virulence. Using Thin Layer Chromatography overlay assays, lactonolysis, and colorimetric quantification, the bioactive compound was inferred to be a chemically modified AHL-like compound or a diketopiperazine-like molecule, potentially involved in biofilm formation in <i>H. saccharovorum</i> CSM52. This study offers new insights into putative QS mechanisms in haloarchaea and their potential role in interspecies communication and coordination, thereby enriching our understanding of microbial interactions in diverse environments.
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spelling doaj.art-81fb0f41756d4cfbb7c2c804a1e919342023-11-18T02:34:18ZengMDPI AGMicroorganisms2076-26072023-05-01115127110.3390/microorganisms11051271Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and BacteriaThomas P. Thompson0Alessandro Busetti1Brendan F. Gilmore2Biofilm Research Group, School of Pharmacy, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, UKBiofilm Research Group, School of Pharmacy, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, UKBiofilm Research Group, School of Pharmacy, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, UKQuorum Sensing (QS) is a well-studied intercellular communication mechanism in bacteria, regulating collective behaviors such as biofilm formation, virulence, and antibiotic resistance. However, cell–cell signaling in haloarchaea remains largely unexplored. The coexistence of bacteria and archaea in various environments, coupled with the known cell–cell signaling mechanisms in both prokaryotic and eukaryotic microorganisms and the presence of cell–cell signaling mechanisms in both prokaryotic and eukaryotic microorganisms, suggests a possibility for haloarchaea to possess analogous cell–cell signaling or QS systems. Recently, N-acylhomoserine lactone (AHL)-like compounds were identified in haloarchaea; yet, their precise role—for example, persister cell formation—remains ambiguous. This study investigated the capacity of crude supernatant extract from the haloarchaeon <i>Halorubrum saccharovorum</i> CSM52 to stimulate bacterial AHL-dependent QS phenotypes using bioreporter strains. Our findings reveal that these crude extracts induced several AHL-dependent bioreporters and modulated pyocyanin and pyoverdine production in <i>Pseudomonas aeruginosa</i>. Importantly, our study suggests cross-domain communication between archaea and bacterial pathogens, providing evidence for archaea potentially influencing bacterial virulence. Using Thin Layer Chromatography overlay assays, lactonolysis, and colorimetric quantification, the bioactive compound was inferred to be a chemically modified AHL-like compound or a diketopiperazine-like molecule, potentially involved in biofilm formation in <i>H. saccharovorum</i> CSM52. This study offers new insights into putative QS mechanisms in haloarchaea and their potential role in interspecies communication and coordination, thereby enriching our understanding of microbial interactions in diverse environments.https://www.mdpi.com/2076-2607/11/5/1271quorum sensingarchaeabiofilmN-acyl homoserine lactoneshalophiles
spellingShingle Thomas P. Thompson
Alessandro Busetti
Brendan F. Gilmore
Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria
Microorganisms
quorum sensing
archaea
biofilm
N-acyl homoserine lactones
halophiles
title Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria
title_full Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria
title_fullStr Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria
title_full_unstemmed Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria
title_short Quorum Sensing in <i>Halorubrum saccharovorum</i> Facilitates Cross-Domain Signaling between Archaea and Bacteria
title_sort quorum sensing in i halorubrum saccharovorum i facilitates cross domain signaling between archaea and bacteria
topic quorum sensing
archaea
biofilm
N-acyl homoserine lactones
halophiles
url https://www.mdpi.com/2076-2607/11/5/1271
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AT alessandrobusetti quorumsensinginihalorubrumsaccharovorumifacilitatescrossdomainsignalingbetweenarchaeaandbacteria
AT brendanfgilmore quorumsensinginihalorubrumsaccharovorumifacilitatescrossdomainsignalingbetweenarchaeaandbacteria