Low spatial structure and selection against secreted virulence factors attenuates pathogenicity in <i>Pseudomonas aeruginosa</i>

Granato, Elisa T.; Ziegenhain, Christoph; Marvig, Rasmus Lykke; Kümmerli, Rolf

doi:10.1038/s41396-018-0231-9

Cited by 46 publications

(62 citation statements)

References 78 publications

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“…Bacteria that shift between highly structured and poorly structured environments can cope with this using genetic regulation. For example, Pseudomonas aeruginosa decreases the production of extracellular proteases and toxins in unstructured habitats leading to a loss of virulence 47 . Bacteria may also evolve mechanisms to tackle directly the exploitation of extracellular proteins by non-producers or rapid protein diffusion in poorly structured habitats.…”

Section: Discussionmentioning

confidence: 99%

Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria

García-Garcerá

Rocha

2020

Nat Commun

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We test the hypothesis that the frequency and cost of extracellular proteins produced by bacteria, which often depend on cooperative processes, vary with habitat structure and community diversity. The integration of the environmental distribution of bacteria (using 16S datasets) and their genomes shows that bacteria living in more structured habitats encode more extracellular proteins. In contrast, the effect of community diversity depends on protein function: it's positive for proteins implicated in antagonistic interactions and negative for those involved in nutrient acquisition. Extracellular proteins are costly and endure stronger selective pressure for low cost and for low diffusivity in less structured habitats and in more diverse communities. Finally, Bacteria found in multiple types of habitats, including hostassociated generalists, encode more extracellular proteins than niche-restricted bacteria. These results show that ecological variables, notably habitat structure and community diversity, shape the evolution of the repertoires of genes encoding extracellular proteins and thus affect the ability of bacteria to manipulate their environment.

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Section: Discussionmentioning

confidence: 99%

Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria

García-Garcerá

Rocha

2020

Nat Commun

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“…They constitute virulence factors in infections (Miethke and Marahiel 2007;Cassat and Skaar 2013), remediate heavy-metal polluted environments (Braud et al 2010;Hesse et al 2018), and drive community dynamics by supressing the growth of competitors (Butaitė et al 2017) or benefiting close relatives through cooperative molecule sharing (Griffin et al 2004;Weigert and Kümmerli 2017). Especially the observation that the secretion of siderophores can constitute a cooperative act, benefiting individuals other than the producers, has attracted enormous attention (Griffin et al 2004;Cordero et al 2012;Julou et al 2013;Andersen et al 2015;Tekwa et al 2017;Vasse et al 2017;Granato et al 2018). The key question in this context is how cooperative siderophore secretion can be evolutionarily maintained, given that siderophore-negative cheater mutants can arise and freeride on the public goods produced by others (West et al 2006;Özkaya et al 2017).…”

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confidence: 99%

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

et al. 2019

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Explaining how cooperation can persist in the presence of cheaters, exploiting the cooperative acts, is a challenge for evolutionary biology. Microbial systems have proved extremely useful to test evolutionary theory and identify mechanisms maintaining cooperation. One of the most widely studied system is the secretion and sharing of iron‐scavenging siderophores by Pseudomonas bacteria, with many insights gained from this system now being considered as hallmarks of bacterial cooperation. Here, we introduce siderophore secretion by the bacterium Burkholderia cenocepacia H111 as a novel parallel study system, and show that this system behaves differently. For ornibactin, the main siderophore of this species, we discovered a novel mechanism of how cheating can be prevented. Particularly, we found that secreted ornibactin cannot be exploited by ornibactin‐defective mutants because ornibactin receptor and synthesis genes are co‐expressed from the same operon, such that disruptive mutations in synthesis genes compromise receptor availability required for siderophore uptake and cheating. For pyochelin, the secondary siderophore of this species, we found that cheating was possible, but the relative success of cheaters was positive frequency dependent, thus diametrically opposite to the Pseudomonas and other microbial systems. Altogether, our results highlight that expanding our repertoire of microbial study systems leads to new discoveries and suggest that there is an enormous diversity of social interactions out there in nature, and we might have only looked at the tip of the iceberg so far.

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“…They constitute virulence factors in infections 1,3 ; remediate heavy-metal polluted environments 4,5 ; and drive community dynamics by supressing the growth of competitors 6 or benefiting close relatives through cooperative molecule sharing 7,8 . Especially the observation that the secretion of siderophores can constitute a cooperative act, benefiting individuals other than the producers, has attracted enormous interdisciplinary attention 7,9–14 . The key question in this context is how cooperative siderophore secretion can be evolutionarily maintained, given that siderophore-negative cheater mutants can arise and freeride on the public goods produced by others 15,16 .…”

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confidence: 99%

Genetic architecture constrains exploitation of siderophore cooperation inBurkholderia cenocepacia

Sathe

Mathew

Agnoli

et al. 2019

Preprint

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13 14 2Explaining how cooperation can persist in the presence of cheaters, exploiting the 15 cooperative acts, is a challenge for evolutionary biology. While microbial systems have 16 proved extremely useful to test evolutionary theory and identify mechanisms maintaining 17 cooperation, our knowledge is often limited to insights gained from a few model 18 organisms. Here, we introduce siderophore secretion by the bacterium Burkholderia 19 cenocepacia as a novel study system. Using a combination of phenotypic and competition 20 assays we found that ornibactin, the main siderophore used for iron scavenging in this 21 species, is secreted into the media, can be shared as public good between cells, but cannot 22 be exploited by ornibactin-defective mutants. Molecular analysis revealed that cheating 23 is compromised because the ornibactin receptor gene and genes involved in ornibactin 24 synthesis are co-expressed from the same operon, such that disruptive mutations in the 25 upstream synthesis genes compromise receptor availability. To prove that it is the genetic 26 architecture of the siderophore locus that prevents cheating, we broke the linked traits 27 by expressing the ornibactin receptor from a plasmid, a measure that turned the 28 ornibactin mutant into a functional cheater. A literature survey across Burkholderia 29 species suggests that the genetic linkage independently broke over evolutionary time 30 scales in several lineages, indicating that cheating and countermeasures might be under 31 selection. Altogether, our results highlight that expanding our repertoire of microbial 32 study systems leads to new discoveries and reinforce the view that social interactions 33 shape evolutionary dynamics in microbial communities. 34 35 3Siderophores are secondary metabolites secreted by bacteria to scavenge insoluble and host-36 bound iron from the environment 1,2 . Siderophores are of major ecological importance as they 37 fulfil a wide range of functions. They constitute virulence factors in infections 1,3 ; remediate 38 heavy-metal polluted environments 4,5 ; and drive community dynamics by supressing the 39 growth of competitors 6 or benefiting close relatives through cooperative molecule sharing 7,8 . 40 Especially the observation that the secretion of siderophores can constitute a cooperative act, 41 benefiting individuals other than the producers, has attracted enormous interdisciplinary 42 attention 7,[9][10][11][12][13][14] . The key question in this context is how cooperative siderophore secretion can be 43 evolutionarily maintained, given that siderophore-negative cheater mutants can arise and 44 freeride on the public goods produced by others 15,16 . A large body of work has tackled this 45 question and revealed that cheating and cheater control are major determinants of bacterial 46 population dynamics in infections and in laboratory and natural communities 6,9,11,[17][18][19] . 47

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Low spatial structure and selection against secreted virulence factors attenuates pathogenicity in Pseudomonas aeruginosa

Cited by 46 publications

References 78 publications

Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria

Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

Genetic architecture constrains exploitation of siderophore cooperation inBurkholderia cenocepacia

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