Literature DB >> 26216986

Socially mediated induction and suppression of antibiosis during bacterial coexistence.

Monica I Abrudan1, Fokko Smakman2, Ard Jan Grimbergen3, Sanne Westhoff2, Eric L Miller1, Gilles P van Wezel4, Daniel E Rozen5.   

Abstract

Despite their importance for humans, there is little consensus on the function of antibiotics in nature for the bacteria that produce them. Classical explanations suggest that bacteria use antibiotics as weapons to kill or inhibit competitors, whereas a recent alternative hypothesis states that antibiotics are signals that coordinate cooperative social interactions between coexisting bacteria. Here we distinguish these hypotheses in the prolific antibiotic-producing genus Streptomyces and provide strong evidence that antibiotics are weapons whose expression is significantly influenced by social and competitive interactions between competing strains. We show that cells induce facultative responses to cues produced by competitors by (i) increasing their own antibiotic production, thereby decreasing costs associated with constitutive synthesis of these expensive products, and (ii) by suppressing antibiotic production in competitors, thereby reducing direct threats to themselves. These results thus show that although antibiotic production is profoundly social, it is emphatically not cooperative. Using computer simulations, we next show that these facultative strategies can facilitate the maintenance of biodiversity in a community context by converting lethal interactions between neighboring colonies to neutral interactions where neither strain excludes the other. Thus, just as bacteriocins can lead to increased diversity via rock-paper-scissors dynamics, so too can antibiotics via elicitation and suppression. Our results reveal that social interactions are crucial for understanding antibiosis and bacterial community dynamics, and highlight the potential of interbacterial interactions for novel drug discovery by eliciting pathways that mediate interference competition.

Entities:  

Keywords:  Streptomyces; antibiotics; competition sensing; microbial ecology; sociomicrobiology

Mesh:

Substances:

Year:  2015        PMID: 26216986      PMCID: PMC4568218          DOI: 10.1073/pnas.1504076112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  35 in total

1.  Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors.

Authors:  Benjamin Kerr; Margaret A Riley; Marcus W Feldman; Brendan J M Bohannan
Journal:  Nature       Date:  2002-07-11       Impact factor: 49.962

Review 2.  Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria.

Authors:  Jos M Raaijmakers; Mark Mazzola
Journal:  Annu Rev Phytopathol       Date:  2012-06-06       Impact factor: 13.078

Review 3.  The world of subinhibitory antibiotic concentrations.

Authors:  Julian Davies; George B Spiegelman; Grace Yim
Journal:  Curr Opin Microbiol       Date:  2006-08-30       Impact factor: 7.934

Review 4.  Evolutionary theory of bacterial quorum sensing: when is a signal not a signal?

Authors:  Stephen P Diggle; Andy Gardner; Stuart A West; Ashleigh S Griffin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2007-07-29       Impact factor: 6.237

Review 5.  Triggers and cues that activate antibiotic production by actinomycetes.

Authors:  Hua Zhu; Stephanie K Sandiford; Gilles P van Wezel
Journal:  J Ind Microbiol Biotechnol       Date:  2013-08-02       Impact factor: 3.346

Review 6.  Antibiotics as signals that trigger specific bacterial responses.

Authors:  Alicia Fajardo; José L Martínez
Journal:  Curr Opin Microbiol       Date:  2008-03-25       Impact factor: 7.934

7.  Microbiology. Alternative actions for antibiotics.

Authors:  William Croft Ratcliff; Robert Ford Denison
Journal:  Science       Date:  2011-04-29       Impact factor: 47.728

8.  Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces.

Authors:  Sébastien Rigali; Fritz Titgemeyer; Sharief Barends; Suzanne Mulder; Andreas W Thomae; David A Hopwood; Gilles P van Wezel
Journal:  EMBO Rep       Date:  2008-05-30       Impact factor: 8.807

9.  Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.

Authors:  Matthew Kearse; Richard Moir; Amy Wilson; Steven Stones-Havas; Matthew Cheung; Shane Sturrock; Simon Buxton; Alex Cooper; Sidney Markowitz; Chris Duran; Tobias Thierer; Bruce Ashton; Peter Meintjes; Alexei Drummond
Journal:  Bioinformatics       Date:  2012-04-27       Impact factor: 6.937

10.  Global biogeographic sampling of bacterial secondary metabolism.

Authors:  Zachary Charlop-Powers; Jeremy G Owen; Boojala Vijay B Reddy; Melinda A Ternei; Denise O Guimarães; Ulysses A de Frias; Monica T Pupo; Prudy Seepe; Zhiyang Feng; Sean F Brady
Journal:  Elife       Date:  2015-01-19       Impact factor: 8.140

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  67 in total

Review 1.  Culture-independent discovery of natural products from soil metagenomes.

Authors:  Micah Katz; Bradley M Hover; Sean F Brady
Journal:  J Ind Microbiol Biotechnol       Date:  2015-11-19       Impact factor: 3.346

2.  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

Review 3.  Taxonomy, Physiology, and Natural Products of Actinobacteria.

Authors:  Essaid Ait Barka; Parul Vatsa; Lisa Sanchez; Nathalie Gaveau-Vaillant; Cedric Jacquard; Jan P Meier-Kolthoff; Hans-Peter Klenk; Christophe Clément; Yder Ouhdouch; Gilles P van Wezel
Journal:  Microbiol Mol Biol Rev       Date:  2015-11-25       Impact factor: 11.056

4.  Competitive inter-species interactions underlie the increased antimicrobial tolerance in multispecies brewery biofilms.

Authors:  Ilse Parijs; Hans P Steenackers
Journal:  ISME J       Date:  2018-06-01       Impact factor: 10.302

5.  Uncertainty quantification of the effects of biotic interactions on community dynamics from nonlinear time-series data.

Authors:  Simone Cenci; Serguei Saavedra
Journal:  J R Soc Interface       Date:  2018-10-31       Impact factor: 4.118

Review 6.  Emergent Properties of Microbial Activity in Heterogeneous Soil Microenvironments: Different Research Approaches Are Slowly Converging, Yet Major Challenges Remain.

Authors:  Philippe C Baveye; Wilfred Otten; Alexandra Kravchenko; María Balseiro-Romero; Éléonore Beckers; Maha Chalhoub; Christophe Darnault; Thilo Eickhorst; Patricia Garnier; Simona Hapca; Serkan Kiranyaz; Olivier Monga; Carsten W Mueller; Naoise Nunan; Valérie Pot; Steffen Schlüter; Hannes Schmidt; Hans-Jörg Vogel
Journal:  Front Microbiol       Date:  2018-08-27       Impact factor: 5.640

7.  Chemoreactive Natural Products that Afford Resistance Against Disparate Antibiotics and Toxins.

Authors:  Lin Du; Jianlan You; Kenneth M Nicholas; Robert H Cichewicz
Journal:  Angew Chem Int Ed Engl       Date:  2016-03-01       Impact factor: 15.336

8.  Cheating fosters species co-existence in well-mixed bacterial communities.

Authors:  Anne Leinweber; R Fredrik Inglis; Rolf Kümmerli
Journal:  ISME J       Date:  2017-01-06       Impact factor: 10.302

Review 9.  Laboratory Evolution of Microbial Interactions in Bacterial Biofilms.

Authors:  Marivic Martin; Theresa Hölscher; Anna Dragoš; Vaughn S Cooper; Ákos T Kovács
Journal:  J Bacteriol       Date:  2016-09-09       Impact factor: 3.490

Review 10.  Spatial structure, cooperation and competition in biofilms.

Authors:  Carey D Nadell; Knut Drescher; Kevin R Foster
Journal:  Nat Rev Microbiol       Date:  2016-07-25       Impact factor: 60.633

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