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Environmental determinants of pyoverdine production, exploitation and competition in natural Pseudomonas communities


Butaitė, Elena; Kramer, Jos; Wyder, Stefan; Kümmerli, Rolf (2018). Environmental determinants of pyoverdine production, exploitation and competition in natural Pseudomonas communities. Environmental Microbiology, 20(10):3629-3642.

Abstract

Many bacteria rely on the secretion of siderophores to scavenge iron from the environment. Laboratory studies revealed that abiotic and biotic factors together determine how much siderophores bacteria make, and whether siderophores can be exploited by non‐producing cheaters or be deployed by producers to inhibit competitors. Here, we explore whether these insights apply to natural communities, by comparing the production of the siderophore pyoverdine among 930 Pseudomonas strains from 48 soil and pond communities. We found that pH, iron content, carbon concentration, and community diversity determine pyoverdine production levels, and the extent to which strains are either stimulated or inhibited by heterologous (non‐self) pyoverdines. While pyoverdine non‐producers occurred in both habitats, their prevalence was higher in soils. Environmental and genetic analysis suggest that non‐producers can evolve as cheaters, exploiting heterologous pyoverdine, but also due to pyoverdine disuse in environments with increased iron availability. Overall, we found that environmental factors explained between‐strain variation in pyoverdine production much better in soils than in ponds, presumably because high strain mixing in ponds prevents local adaption. Our study sheds light on the complexity of natural bacterial communities, and provides first insights into the multivariate nature of siderophore‐based iron acquisition and competition among environmental pseudomonads.

Abstract

Many bacteria rely on the secretion of siderophores to scavenge iron from the environment. Laboratory studies revealed that abiotic and biotic factors together determine how much siderophores bacteria make, and whether siderophores can be exploited by non‐producing cheaters or be deployed by producers to inhibit competitors. Here, we explore whether these insights apply to natural communities, by comparing the production of the siderophore pyoverdine among 930 Pseudomonas strains from 48 soil and pond communities. We found that pH, iron content, carbon concentration, and community diversity determine pyoverdine production levels, and the extent to which strains are either stimulated or inhibited by heterologous (non‐self) pyoverdines. While pyoverdine non‐producers occurred in both habitats, their prevalence was higher in soils. Environmental and genetic analysis suggest that non‐producers can evolve as cheaters, exploiting heterologous pyoverdine, but also due to pyoverdine disuse in environments with increased iron availability. Overall, we found that environmental factors explained between‐strain variation in pyoverdine production much better in soils than in ponds, presumably because high strain mixing in ponds prevents local adaption. Our study sheds light on the complexity of natural bacterial communities, and provides first insights into the multivariate nature of siderophore‐based iron acquisition and competition among environmental pseudomonads.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
08 Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:580 Plants (Botany)
Uncontrolled Keywords:Ecology, Evolution, Behavior and Systematics, Microbiology
Language:English
Date:1 October 2018
Deposited On:05 Feb 2019 14:41
Last Modified:25 Sep 2019 00:05
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:1462-2912
OA Status:Closed
Publisher DOI:https://doi.org/10.1111/1462-2920.14355
Project Information:
  • : FunderSNSF
  • : Grant IDPP00P3_165835
  • : Project TitleCooperation and competition in bacteria: extension
  • : FunderSNSF
  • : Grant IDPP00P3_139164
  • : Project TitleCooperation and competition in bacteria: analyses from the single-cell to the community level

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