Literature DB >> 22763647

Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model.

Josephine R Chandler1, Silja Heilmann, John E Mittler, E Peter Greenberg.   

Abstract

Many Proteobacteria use acyl-homoserine lactone (AHL)-mediated quorum sensing to activate the production of antibiotics at high cell density. Extracellular factors like antibiotics can be considered public goods shared by individuals within a group. Quorum-sensing control of antibiotic production may be important for protecting a niche or competing for limited resources in mixed bacterial communities. To begin to investigate the role of quorum sensing in interspecies competition, we developed a dual-species co-culture model using the soil saprophytes Burkholderia thailandensis (Bt) and Chromobacterium violaceum (Cv). These bacteria require quorum sensing to activate the production of antimicrobial factors that inhibit growth of the other species. We demonstrate that quorum-sensing-dependent antimicrobials can provide a competitive advantage to either Bt or Cv by inhibiting growth of the other species in co-culture. Although the quorum-sensing signals differ for each species, we show that the promiscuous signal receptor encoded by Cv can sense signals produced by Bt, and that this ability to eavesdrop on Bt can provide Cv an advantage in certain situations. We use an in silico approach to investigate the effect of eavesdropping in competition, and show conditions where early activation of antibiotic production resulting from eavesdropping can promote competitiveness. Our work supports the idea that quorum sensing is important for interspecies competition and that promiscuous signal receptors allow eavesdropping on competitors in mixed microbial habitats.

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Year:  2012        PMID: 22763647      PMCID: PMC3504959          DOI: 10.1038/ismej.2012.69

Source DB:  PubMed          Journal:  ISME J        ISSN: 1751-7362            Impact factor:   10.302


  49 in total

Review 1.  Quorum sensing in the Burkholderia cepacia complex.

Authors:  Vittorio Venturi; Arianna Friscina; Iris Bertani; Giulia Devescovi; Claudio Aguilar
Journal:  Res Microbiol       Date:  2004-05       Impact factor: 3.992

Review 2.  Quorum sensing: cell-to-cell communication in bacteria.

Authors:  Christopher M Waters; Bonnie L Bassler
Journal:  Annu Rev Cell Dev Biol       Date:  2005       Impact factor: 13.827

3.  Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals.

Authors:  Yaya Cui; Asita Chatterjee; Hiroaki Hasegawa; Arun K Chatterjee
Journal:  J Bacteriol       Date:  2006-07       Impact factor: 3.490

4.  A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa.

Authors:  Joao B Xavier; Wook Kim; Kevin R Foster
Journal:  Mol Microbiol       Date:  2010-11-02       Impact factor: 3.501

5.  Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia.

Authors:  Nathan A Ahlgren; Caroline S Harwood; Amy L Schaefer; Eric Giraud; E Peter Greenberg
Journal:  Proc Natl Acad Sci U S A       Date:  2011-04-06       Impact factor: 11.205

Review 6.  Bacterial competition: surviving and thriving in the microbial jungle.

Authors:  Michael E Hibbing; Clay Fuqua; Matthew R Parsek; S Brook Peterson
Journal:  Nat Rev Microbiol       Date:  2010-01       Impact factor: 60.633

7.  The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability.

Authors: 
Journal:  Proc Natl Acad Sci U S A       Date:  2003-09-18       Impact factor: 11.205

8.  Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis.

Authors:  Breck A Duerkop; John Varga; Josephine R Chandler; Snow Brook Peterson; Jake P Herman; Mair E A Churchill; Matthew R Parsek; William C Nierman; E Peter Greenberg
Journal:  J Bacteriol       Date:  2009-04-17       Impact factor: 3.490

9.  A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity.

Authors:  Lee R Swem; Danielle L Swem; Colleen T O'Loughlin; Raleene Gatmaitan; Bixiao Zhao; Scott M Ulrich; Bonnie L Bassler
Journal:  Mol Cell       Date:  2009-07-31       Impact factor: 17.970

10.  Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy.

Authors:  P C Seed; L Passador; B H Iglewski
Journal:  J Bacteriol       Date:  1995-02       Impact factor: 3.490

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  40 in total

1.  Antibiotics and the art of bacterial war.

Authors:  Daniel M Cornforth; Kevin R Foster
Journal:  Proc Natl Acad Sci U S A       Date:  2015-08-24       Impact factor: 11.205

2.  Emergence of collective territorial defense in bacterial communities: horizontal gene transfer can stabilize microbiomes.

Authors:  János Juhász; Attila Kertész-Farkas; Dóra Szabó; Sándor Pongor
Journal:  PLoS One       Date:  2014-04-22       Impact factor: 3.240

3.  The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota.

Authors:  Jean-Christophe Lagier; Perrine Hugon; Saber Khelaifia; Pierre-Edouard Fournier; Bernard La Scola; Didier Raoult
Journal:  Clin Microbiol Rev       Date:  2015-01       Impact factor: 26.132

Review 4.  Flexibility and Adaptability of Quorum Sensing in Nature.

Authors:  Rebecca D Prescott; Alan W Decho
Journal:  Trends Microbiol       Date:  2020-01-27       Impact factor: 17.079

5.  The Chemistry and Biology of Bactobolin: A 10-Year Collaboration with Natural Product Chemist Extraordinaire Jon Clardy.

Authors:  E Peter Greenberg; Josephine R Chandler; Mohammad R Seyedsayamdost
Journal:  J Nat Prod       Date:  2020-02-27       Impact factor: 4.050

Review 6.  Symbiosis-inspired approaches to antibiotic discovery.

Authors:  Navid Adnani; Scott R Rajski; Tim S Bugni
Journal:  Nat Prod Rep       Date:  2017-07-06       Impact factor: 13.423

7.  Microbial population dynamics in the hemolymph of Manduca sexta infected with Xenorhabdus nematophila and the entomopathogenic nematode Steinernema carpocapsae.

Authors:  Swati Singh; Jordan M Reese; Angel M Casanova-Torres; Heidi Goodrich-Blair; Steven Forst
Journal:  Appl Environ Microbiol       Date:  2014-05-09       Impact factor: 4.792

8.  A Burkholderia thailandensis Acyl-Homoserine Lactone-Independent Orphan LuxR Homolog That Activates Production of the Cytotoxin Malleilactone.

Authors:  Thao T Truong; Mohammad Seyedsayamdost; E Peter Greenberg; Josephine R Chandler
Journal:  J Bacteriol       Date:  2015-08-17       Impact factor: 3.490

9.  Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress.

Authors:  Eunhye Goo; Charlotte D Majerczyk; Jae Hyung An; Josephine R Chandler; Young-Su Seo; Hyeonheui Ham; Jae Yun Lim; Hongsup Kim; Bongsoo Lee; Moon Sun Jang; E Peter Greenberg; Ingyu Hwang
Journal:  Proc Natl Acad Sci U S A       Date:  2012-11-12       Impact factor: 11.205

10.  Quorum-sensing control of antibiotic resistance stabilizes cooperation in Chromobacterium violaceum.

Authors:  Kara C Evans; Saida Benomar; Lennel A Camuy-Vélez; Ellen B Nasseri; Xiaofei Wang; Benjamin Neuenswander; Josephine R Chandler
Journal:  ISME J       Date:  2018-01-26       Impact factor: 10.302

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