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Siderophores drive invasion dynamics in bacterial communities through their dual role as public good versus public bad


Figueiredo, Alexandre R T; Özkaya, Özhan; Kümmerli, Rolf; Kramer, Jos (2022). Siderophores drive invasion dynamics in bacterial communities through their dual role as public good versus public bad. Ecology Letters, 25(1):138-150.

Abstract

Microbial invasions can compromise ecosystem services and spur dysbiosis and disease in hosts. Nevertheless, the mechanisms determining invasion outcomes often remain unclear. Here, we examine the role of iron-scavenging siderophores in driving invasions of Pseudomonas aeruginosa into resident communities of environmental pseudomonads. Siderophores can be 'public goods' by delivering iron to individuals possessing matching receptors; but they can also be 'public bads' by withholding iron from competitors lacking these receptors. Accordingly, siderophores should either promote or impede invasion, depending on their effects on invader and resident growth. Using supernatant feeding and invasion assays, we show that invasion success indeed increased when the invader could use its siderophores to inhibit (public bad) rather than stimulate (public good) resident growth. Conversely, invasion success decreased the more the invader was inhibited by the residents' siderophores. Our findings identify siderophores as a major driver of invasion dynamics in bacterial communities under iron-limited conditions.

Abstract

Microbial invasions can compromise ecosystem services and spur dysbiosis and disease in hosts. Nevertheless, the mechanisms determining invasion outcomes often remain unclear. Here, we examine the role of iron-scavenging siderophores in driving invasions of Pseudomonas aeruginosa into resident communities of environmental pseudomonads. Siderophores can be 'public goods' by delivering iron to individuals possessing matching receptors; but they can also be 'public bads' by withholding iron from competitors lacking these receptors. Accordingly, siderophores should either promote or impede invasion, depending on their effects on invader and resident growth. Using supernatant feeding and invasion assays, we show that invasion success indeed increased when the invader could use its siderophores to inhibit (public bad) rather than stimulate (public good) resident growth. Conversely, invasion success decreased the more the invader was inhibited by the residents' siderophores. Our findings identify siderophores as a major driver of invasion dynamics in bacterial communities under iron-limited conditions.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
07 Faculty of Science > Department of Quantitative Biomedicine
08 Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:610 Medicine & health
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Uncontrolled Keywords:Ecology, Evolution, Behavior and Systematics
Language:English
Date:1 January 2022
Deposited On:01 Feb 2022 12:23
Last Modified:26 Feb 2024 02:46
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:1461-023X
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1111/ele.13912
PubMed ID:34753204
Project Information:
  • : FunderH2020
  • : Grant ID681295
  • : Project TitleBactInd - Bacterial cooperation at the individual cell level
  • : FunderSNSF
  • : Grant ID31003A_182499
  • : Project TitleAn evolutionary ecology approach to disarm bacterial pathogens, control infections, and understand polymicrobial interactions inside hosts
  • Content: Published Version
  • Language: English
  • Licence: Creative Commons: Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)