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Title: Bioactive exometabolites drive maintenance competition in simple bacterial communities

Journal Article · · mSystems

During prolonged resource limitation, bacterial cells can persist in metabolically active states of non-growth. These maintenance periods, such as those experienced in stationary phase, can include upregulation of secondary metabolism and release of exometabolites into the local environment. As resource limitation is common in many environmental microbial habitats, we hypothesized that neighboring bacterial populations employ exometabolites to compete or cooperate during maintenance and that these exometabolite-facilitated interactions can drive community outcomes. Here, we evaluated the consequences of exometabolite interactions over the stationary phase among three environmental strains: Burkholderia thailandensis E264, Chromobacterium subtsugae ATCC 31532, and Pseudomonas syringae pv. tomato DC3000. We assembled them into synthetic communities that only permitted chemical interactions. We compared the responses (transcripts) and outputs (exometabolites) of each member with and without neighbors. We found that transcriptional dynamics were changed with different neighbors and that some of these changes were coordinated between members. The dominant competitor B. thailandensis consistently upregulated biosynthetic gene clusters to produce bioactive exometabolites for both exploitative and interference competition. These results demonstrate that competition strategies during maintenance can contribute to community-level outcomes. It also suggests that the traditional concept of defining competitiveness by growth outcomes may be narrow and that maintenance competition could be an additional or alternative measure.

Research Organization:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2471093
Journal Information:
mSystems, Journal Name: mSystems Journal Issue: 4 Vol. 9; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (97)

Feast/famine growth environments and activated sludge population selection journal May 1985
ggplot2 book January 2016
Mixed fermentation for natural product drug discovery journal May 2009
Triggers and cues that activate antibiotic production by actinomycetes journal August 2013
Temporal variability in detritus resource maintains diversity of bacterial communities journal May 2008
Modeling the Overproduction of Ribosomes when Antibacterial Drugs Act on Cells journal February 2016
A Common Mechanism of Cellular Death Induced by Bactericidal Antibiotics journal September 2007
Higher-Order Interaction between Species Inhibits Bacterial Invasion of a Phototroph-Predator Microbial Community journal December 2019
Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment journal August 2015
Competition, Not Cooperation, Dominates Interactions among Culturable Microbial Species journal October 2012
The Antibacterial Threaded-lasso Peptide Capistruin Inhibits Bacterial RNA Polymerase journal October 2011
Bactobolin A Binds to a Site on the 70S Ribosome Distinct from Previously Seen Antibiotics journal February 2015
Bacterial competition in serial transfer culture journal February 2011
Synthetic microbial communities journal April 2014
Dividing subpopulation of Escherichia coli in stationary phase journal April 2020
The Ecology and Evolution of Microbial Competition journal October 2016
Effects of chloramphenicol on the transcriptional activities of ribosomal RNA and ribosomal protein genes in Escherichia coli journal December 1976
Mapping the Trimethoprim-Induced Secondary Metabolome of Burkholderia thailandensis journal July 2016
Global Awakening of Cryptic Biosynthetic Gene Clusters in Burkholderia thailandensis journal November 2017
Identifying Small Molecules via High Resolution Mass Spectrometry: Communicating Confidence journal February 2014
Induced Biosynthesis of Cryptic Polyketide Metabolites in a Burkholderia thailandensis Quorum Sensing Mutant journal September 2010
Malleilactone, a Polyketide Synthase-Derived Virulence Factor Encoded by the Cryptic Secondary Metabolome of Burkholderia pseudomallei Group Pathogens journal August 2012
Isolation and Structural Characterization of Capistruin, a Lasso Peptide Predicted from the Genome Sequence of Burkholderia thailandensis E264 journal August 2008
What is microbial community ecology? journal August 2009
Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model journal July 2012
Temperature-induced behavioral switches in a bacterial coral pathogen journal December 2015
Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli journal January 2007
Minimum Information about a Biosynthetic Gene cluster journal August 2015
Microbial metabolic exchange—the chemotype-to-phenotype link journal December 2011
Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour journal September 2016
Metabolic footprinting and systems biology: the medium is the message journal June 2005
Physiological heterogeneity in biofilms journal March 2008
Bacterial competition: surviving and thriving in the microbial jungle journal November 2009
Competition sensing: the social side of bacterial stress responses journal March 2013
The regulation of bacterial transcription initiation journal January 2004
Quorum-sensing control of antibiotic resistance stabilizes cooperation in Chromobacterium violaceum journal January 2018
Species-specific transcriptomic network inference of interspecies interactions journal May 2018
Interspecies bacterial competition regulates community assembly in the C. elegans intestine journal February 2021
Discovery of scmR as a global regulator of secondary metabolism and virulence in Burkholderia thailandensis E264 journal March 2017
Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts journal September 2017
The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000 journal August 2003
Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics journal December 2002
Partitioning of Resources and the Outcome of Interspecific Competition: A Model and Some General Considerations journal March 1973
A Critical Review of Twenty Years’ Use of the Resource‐Ratio Theory journal April 2005
InterProScan - an integration platform for the signature-recognition methods in InterPro journal September 2001
BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks journal June 2005
rtracklayer: an R package for interfacing with genome browsers journal May 2009
Fifty important research questions in microbial ecology journal April 2017
Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules journal August 2016
antiSMASH 6.0: improving cluster detection and comparison capabilities journal May 2021
MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights journal May 2021
High-throughput functional annotation and data mining with the Blast2GO suite journal April 2008
The genome portal of the Department of Energy Joint Genome Institute: 2014 updates journal November 2013
Network analysis of transcriptomics expands regulatory landscapes in Synechococcus sp. PCC 7002 journal August 2016
Impulse model-based differential expression analysis of time course sequencing data journal August 2018
MIBiG 2.0: a repository for biosynthetic gene clusters of known function journal October 2019
Mathematical modelling of microbes: metabolism, gene expression and growth journal November 2017
Towards a unified study of multiple stressors: divisions and common goals across research disciplines journal May 2020
Note: Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species journal January 1998
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities: Synthetic microbial ecosystems journal December 2013
Stationary phase in gram-negative bacteria journal July 2010
Interspecies modulation of bacterial development through iron competition and siderophore piracy: Xenosiderophores alter development in actinomycetes journal September 2012
The ecology of the microbiome: Networks, competition, and stability journal November 2015
Thailandamide, a Fatty Acid Synthesis Antibiotic That Is Coexpressed with a Resistant Target Gene journal September 2018
Antibiotic Killing of Diversely Generated Populations of Nonreplicating Bacteria journal July 2019
Stable Coexistence of Five Bacterial Strains as a Cellulose-Degrading Community journal November 2005
Quorum-Sensing Control of Antibiotic Synthesis in Burkholderia thailandensis journal April 2009
A Burkholderia thailandensis Acyl-Homoserine Lactone-Independent Orphan LuxR Homolog That Activates Production of the Cytotoxin Malleilactone journal August 2015
The DNA-Binding Protein from Starved Cells (Dps) Utilizes Dual Functions To Defend Cells against Multiple Stresses journal October 2015
Dps Protects Cells against Multiple Stresses during Stationary Phase journal June 2004
Genetic and Transcriptional Analysis of the Siderophore Malleobactin Biosynthesis and Transport Genes in the Human Pathogen Burkholderia pseudomallei K96243 journal February 2006
Multi-Omic Analyses Provide Links between Low-Dose Antibiotic Treatment and Induction of Secondary Metabolism in Burkholderia thailandensis journal February 2020
Toward a Better Understanding of Species Interactions through Network Biology journal June 2019
A Synthetic Community System for Probing Microbial Interactions Driven by Exometabolites journal November 2017
Exometabolite Dynamics over Stationary Phase Reveal Strain-Specific Responses journal December 2020
Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes journal November 2018
Two-Component Signal Transduction journal June 2000
Rules of Engagement: Interspecies Interactions that Regulate Microbial Communities journal October 2008
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data journal July 2010
minet: A R/Bioconductor Package for Inferring Large Transcriptional Networks Using Mutual Information journal October 2008
Burkholderia thailandensis harbors two identical rhl gene clusters responsible for the biosynthesis of rhamnolipids journal December 2009
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Reclassification of Chromobacterium violaceum ATCC 31532 and its quorum biosensor mutant CV026 to Chromobacterium subtsugae journal November 2020
Large-Scale Mapping and Validation of Escherichia coli Transcriptional Regulation from a Compendium of Expression Profiles journal January 2007
High-order interactions distort the functional landscape of microbial consortia journal December 2019
Reshaping Data with the reshape Package journal January 2007
Theoretical Perspectives on Resource Pulses journal March 2008
Welcome to the Tidyverse journal November 2019
Iron Acquisition Mechanisms and Their Role in the Virulence of Burkholderia Species journal November 2017
Microbial responses to multi-factor climate change: effects on soil enzymes journal January 2013
Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters journal April 2015
Interspecies interactions are an integral determinant of microbial community dynamics journal October 2015
Secondary Metabolites Produced during the Germination of Streptomyces coelicolor journal December 2017
Extracellular Microbial Metabolomics: The State of the Art journal August 2017
SQ 26,180, a novel monobactam. I. Taxonomy, fermentation and biological properties. journal January 1982
Integrated culturing, modeling and transcriptomics uncovers complex interactions and emergent behavior in a three-species synthetic gut community journal October 2018