N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities

Bacterial biofilms are important medically, environmentally and industrially and there is a need to understand the processes that govern functional synergy and dynamics of species within biofilm communities. Here, we have used a model, mixed-species biofilm community comprised of Pseudomonas aerugin...

Full description

Bibliographic Details
Main Authors: Sujatha Subramoni, Muhammad Zulfadhly Bin Mohammad Muzaki, Sean C. M. Booth, Staffan Kjelleberg, Scott A. Rice
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2021.646991/full
id doaj-cc606870703d45d3829ffe21c9cc5f11
record_format Article
spelling doaj-cc606870703d45d3829ffe21c9cc5f112021-03-19T15:03:15ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-03-011110.3389/fcimb.2021.646991646991N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm CommunitiesSujatha Subramoni0Muhammad Zulfadhly Bin Mohammad Muzaki1Muhammad Zulfadhly Bin Mohammad Muzaki2Sean C. M. Booth3Staffan Kjelleberg4Staffan Kjelleberg5Scott A. Rice6Scott A. Rice7Scott A. Rice8Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeSchool of Biological Sciences, Nanyang Technological University, Singapore, Singaporeithree Institute, The University of Technology Sydney, Sydney, NSW, AustraliaBacterial biofilms are important medically, environmentally and industrially and there is a need to understand the processes that govern functional synergy and dynamics of species within biofilm communities. Here, we have used a model, mixed-species biofilm community comprised of Pseudomonas aeruginosa PAO1, Pseudomonas protegens Pf-5 and Klebsiella pneumoniae KP1. This biofilm community displays higher biomass and increased resilience to antimicrobial stress conditions such as sodium dodecyl sulfate and tobramycin, compared to monospecies biofilm populations. P. aeruginosa is present at low proportions in the community and yet, it plays a critical role in community function, suggesting it acts as a keystone species in this community. To determine the factors that regulate community composition, we focused on P. aeruginosa because of its pronounced impact on community structure and function. Specifically, we evaluated the role of the N-acyl homoserine lactone (AHL) dependent quorum sensing (QS) system of P. aeruginosa PAO1, which regulates group behaviors including biofilm formation and the production of effector molecules. We found that mixed species biofilms containing P. aeruginosa QS mutants had significantly altered proportions of K. pneumoniae and P. protegens populations compared to mixed species biofilms with the wild type P. aeruginosa. Similarly, inactivation of QS effector genes, e.g. rhlA and pvdR, also governed the relative species proportions. While the absence of QS did not alter the proportions of the two species in dual species biofilms of P. aeruginosa and K. pneumoniae, it resulted in significantly lower proportions of P. aeruginosa in dual species biofilms with P. protegens. These observations suggest that QS plays an important role in modulating community biofilm structure and physiology and affects interspecific interactions.https://www.frontiersin.org/articles/10.3389/fcimb.2021.646991/fullquorum sensingspecies interactionsmultispeciesbiofilmsPseudomonas aeruginosaPseudomonas protegens
collection DOAJ
language English
format Article
sources DOAJ
author Sujatha Subramoni
Muhammad Zulfadhly Bin Mohammad Muzaki
Muhammad Zulfadhly Bin Mohammad Muzaki
Sean C. M. Booth
Staffan Kjelleberg
Staffan Kjelleberg
Scott A. Rice
Scott A. Rice
Scott A. Rice
spellingShingle Sujatha Subramoni
Muhammad Zulfadhly Bin Mohammad Muzaki
Muhammad Zulfadhly Bin Mohammad Muzaki
Sean C. M. Booth
Staffan Kjelleberg
Staffan Kjelleberg
Scott A. Rice
Scott A. Rice
Scott A. Rice
N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities
Frontiers in Cellular and Infection Microbiology
quorum sensing
species interactions
multispecies
biofilms
Pseudomonas aeruginosa
Pseudomonas protegens
author_facet Sujatha Subramoni
Muhammad Zulfadhly Bin Mohammad Muzaki
Muhammad Zulfadhly Bin Mohammad Muzaki
Sean C. M. Booth
Staffan Kjelleberg
Staffan Kjelleberg
Scott A. Rice
Scott A. Rice
Scott A. Rice
author_sort Sujatha Subramoni
title N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities
title_short N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities
title_full N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities
title_fullStr N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities
title_full_unstemmed N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities
title_sort n-acyl homoserine lactone-mediated quorum sensing regulates species interactions in multispecies biofilm communities
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2021-03-01
description Bacterial biofilms are important medically, environmentally and industrially and there is a need to understand the processes that govern functional synergy and dynamics of species within biofilm communities. Here, we have used a model, mixed-species biofilm community comprised of Pseudomonas aeruginosa PAO1, Pseudomonas protegens Pf-5 and Klebsiella pneumoniae KP1. This biofilm community displays higher biomass and increased resilience to antimicrobial stress conditions such as sodium dodecyl sulfate and tobramycin, compared to monospecies biofilm populations. P. aeruginosa is present at low proportions in the community and yet, it plays a critical role in community function, suggesting it acts as a keystone species in this community. To determine the factors that regulate community composition, we focused on P. aeruginosa because of its pronounced impact on community structure and function. Specifically, we evaluated the role of the N-acyl homoserine lactone (AHL) dependent quorum sensing (QS) system of P. aeruginosa PAO1, which regulates group behaviors including biofilm formation and the production of effector molecules. We found that mixed species biofilms containing P. aeruginosa QS mutants had significantly altered proportions of K. pneumoniae and P. protegens populations compared to mixed species biofilms with the wild type P. aeruginosa. Similarly, inactivation of QS effector genes, e.g. rhlA and pvdR, also governed the relative species proportions. While the absence of QS did not alter the proportions of the two species in dual species biofilms of P. aeruginosa and K. pneumoniae, it resulted in significantly lower proportions of P. aeruginosa in dual species biofilms with P. protegens. These observations suggest that QS plays an important role in modulating community biofilm structure and physiology and affects interspecific interactions.
topic quorum sensing
species interactions
multispecies
biofilms
Pseudomonas aeruginosa
Pseudomonas protegens
url https://www.frontiersin.org/articles/10.3389/fcimb.2021.646991/full
work_keys_str_mv AT sujathasubramoni nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT muhammadzulfadhlybinmohammadmuzaki nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT muhammadzulfadhlybinmohammadmuzaki nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT seancmbooth nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT staffankjelleberg nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT staffankjelleberg nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT scottarice nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT scottarice nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
AT scottarice nacylhomoserinelactonemediatedquorumsensingregulatesspeciesinteractionsinmultispeciesbiofilmcommunities
_version_ 1724212926721556480