Siderophore Production by Cystic Fibrosis Isolates of
            <i>Burkholderia cepacia</i>

Darling, P. E.; Chan, M.; Cox, Andrew D.; Sokol, Pamela A.

doi:10.1128/iai.66.2.874-877.1998

Cited by 154 publications

(89 citation statements)

References 21 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The experiments were performed with Burkholderia cenocepacia H111 (LMG 23991), a clinical isolate from a cystic fibrosis patient 54 . This isolate (hereafter referred to as wild type) produces two siderophores, ornibactin and pyochelin 42,55 . This species further possesses a membrane-embedded siderophore-independent iron uptake mechanism 23 , which we did not focus on in this study because its contribution to iron uptake is relatively minor under the culturing conditions used.…”

Section: Methodsmentioning

confidence: 99%

Genetic architecture constrains exploitation of siderophore cooperation inBurkholderia cenocepacia

Sathe

Mathew

Agnoli

et al. 2019

Preprint

View full text Add to dashboard Cite

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

show abstract

Section: Methodsmentioning

confidence: 99%

Genetic architecture constrains exploitation of siderophore cooperation inBurkholderia cenocepacia

Sathe

Mathew

Agnoli

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…The experiments were performed with Burkholderia cenocepacia H111 (LMG 23991), a clinical isolate from a cystic fibrosis patient (Gotschlick et al 2001). This isolate (hereafter referred to as wild type) produces two siderophores, ornibactin, and pyochelin (Darling et al 1998;Sokol et al 1999). This species further possesses a membrane-embedded siderophore-independent iron uptake mechanism (Mathew et al 2014), which we did not focus on in this study, because its contribution to iron uptake is relatively minor under the culturing conditions used.…”

Section: Bacterial Strainsmentioning

confidence: 99%

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

et al. 2019

View full text Add to dashboard Cite

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.

show abstract

“…Siderophore-mediated iron acquisition has been identified as an important virulence factor in members of the genus Burkholderia and was extensively studied in clinical isolates of B. cenocepacia (Thomas, 2007). They often produce two siderophores, pyochelin and ornibactin (Darling et al, 1998;Sokol et al, 1999) and these have been correlated with the ability of these strains to establish and maintain an infection (Sokol et al, 2000;Visser et al, 2004;Uehlinger et al, 2009). Previous studies have also shown that a single functional siderophore system is sufficient for growth of B. cenocepacia Pc715j in iron restricted conditions (Visser et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

A novel siderophore‐independent strategy of iron uptake in the genus Burkholderia

Mathew

Eberl

Carlier

2014

Molecular Microbiology

View full text Add to dashboard Cite

SummaryLike many other bacteria, Burkholderia sp. take up iron in its ferric form via siderophore-dependent transporters. We observed that mutant strains of B. cenocepacia H111 unable to synthesize siderophores did not exhibit any growth defect under iron limited conditions. This finding suggested that this opportunistic pathogen can adopt an alternative iron uptake strategy to compensate for the loss of siderophores. We identified a putative iron uptake locus, ftrBccABCD, in the genome of B. cenocepacia H111, which is also conserved in other members of the genus Burkholderia. Mutants deficient in both siderophore-dependent and FtrBccABCD systems failed to grow under iron-limited conditions and radiolabelled iron transport assays showed that these mutants were impaired in iron uptake. In addition, expression of ftrBccABCD can restore growth of an E. coli strain lacking all known high-affinity iron transport systems under iron-limited conditions. We show that all four proteins encoded by ftrBccABCD are essential for iron uptake. Furthermore, our results indicate that the expression of ftrBccABCD is regulated at the transcriptional level by iron concentration. This study provides evidence of an alternative, siderophore-independent, iron uptake system in Burkholderia species.

show abstract

Siderophore Production by Cystic Fibrosis Isolates of Burkholderia cepacia

Cited by 154 publications

References 21 publications

Genetic architecture constrains exploitation of siderophore cooperation inBurkholderia cenocepacia

Genetic architecture constrains exploitation of siderophore cooperation inBurkholderia cenocepacia

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

A novel siderophore‐independent strategy of iron uptake in the genus Burkholderia

Contact Info

Product

Resources

About