Iron acquisition in the marine actinomycete genus<i>Salinispora</i>is controlled by the desferrioxamine family of siderophores

Roberts, A. W.; Schultz, Andrew W.; Kersten, Roland D.; Dorrestein, Pieter C.; Moore, Bradley S.

doi:10.1111/j.1574-6968.2012.02641.x

Cited by 35 publications

(34 citation statements)

References 53 publications

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“…S. tropica genome sequences maintain two gene clusters predicted to encode siderophore biosynthesis (sid3 and sid4) that are not found in S. arenicola (Supplementary Table S3 and S5), suggesting an additional investment in iron uptake by this species. Although the inactivation of key genes in the S. tropica sid3 and sid4 clusters did not affect growth in iron-limited media (Roberts et al, 2012), these pathways may have a role in the acquisition of other limiting metals (Bellenger et al, 2008) or be regulated by factors other than iron limitation, and thus enhanced siderophore production could help support higher growth rates in this species. The conservation of sid3 and sid4 among all 12 S. tropica strains for which genome sequences were available suggests that there are strong selective pressures to maintain the functions provided by the products of these pathways.…”

Section: Discussionmentioning

confidence: 89%

“…However, two additional siderophore gene clusters (sid3 and sid4) were also identified in S. tropica CNB-440 (Penn et al, 2009). The production of desferrioxamines B and E was later confirmed for both S. tropica and S. arenicola and linked to the des locus (Roberts et al, 2012). A MultiGeneBlast analysis revealed that all 12 S. tropica strains for which genome sequences are available possess all four of the siderophore gene clusters, whereas the 12 S. arenicola genomes chosen for this study only possess the des and sid2 clusters (Supplementary Table S3).…”

Section: Bioinformatic Analysesmentioning

confidence: 93%

“…(Penn et al, 2009;Roberts et al, 2012). On average, 31.3 secondary metabolite gene clusters were identified in the S. arenicola strains in comparison with 23.1 for S. tropica (Supplementary Table S3).…”

Section: Bioinformatic Analysesmentioning

confidence: 99%

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Competitive strategies differentiate closely related species of marine actinobacteria

et al. 2015

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Although competition, niche partitioning, and spatial isolation have been used to describe the ecology and evolution of macro-organisms, it is less clear to what extent these principles account for the extraordinary levels of bacterial diversity observed in nature. Ecological interactions among bacteria are particularly challenging to address due to methodological limitations and uncertainties over how to recognize fundamental units of diversity and link them to the functional traits and evolutionary processes that led to their divergence. Here we show that two closely related marine actinomycete species can be differentiated based on competitive strategies. Using a direct challenge assay to investigate inhibitory interactions with members of the bacterial community, we observed a temporal difference in the onset of inhibition. The majority of inhibitory activity exhibited by Salinispora arenicola occurred early in its growth cycle and was linked to antibiotic production. In contrast, most inhibition by Salinispora tropica occurred later in the growth cycle and was more commonly linked to nutrient depletion or other sources. Comparative genomics support these differences, with S. arenicola containing nearly twice the number of secondary metabolite biosynthetic gene clusters as S. tropica, indicating a greater potential for secondary metabolite production. In contrast, S. tropica is enriched in gene clusters associated with the acquisition of growth-limiting nutrients such as iron. Coupled with differences in growth rates, the results reveal that S. arenicola uses interference competition at the expense of growth, whereas S. tropica preferentially employs a strategy of exploitation competition. The results support the ecological divergence of two co-occurring and closely related species of marine bacteria by providing evidence they have evolved fundamentally different strategies to compete in marine sediments.

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Section: Discussionmentioning

confidence: 89%

Section: Bioinformatic Analysesmentioning

confidence: 93%

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Competitive strategies differentiate closely related species of marine actinobacteria

et al. 2015

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“…The desferrioxamine family, a group of hydroxamate siderophores, 22 includes over 50 congeners, including acylated derivatives have only been detected from Streptomyces strains before. 11b, 23 The staurosporine molecular family 24 consists of a total of 11 members, mainly produced by Salinispora strains, but hydroxystaurosporine was also found in Streptomyces CNQ-149.…”

Section: Resultsmentioning

confidence: 99%

Prioritizing Natural Product Diversity in a Collection of 146 Bacterial Strains Based on Growth and Extraction Protocols

Crüsemann¹,

O’Neill²,

Larson³

et al. 2016

J. Nat. Prod.

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111

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In order to expedite the rapid and efficient discovery and isolation of novel specialized metabolites, whilst minimizing the waste of resources on rediscovery of known compounds, it is crucial to develop efficient approaches for strain prioritization, rapid dereplication, and the assessment of favored cultivation and extraction conditions. Herein we interrogated bacterial strains by systematically evaluating cultivation and extraction parameters with LC-MS/MS analysis and subsequent dereplication through the Global Natural Product Social Molecular Networking (GNPS) platform. The developed method is fast, requiring minimal time and sample material, and is compatible with high throughput extract analysis, thereby streamlining strain prioritization and evaluation of culturing parameters. With this approach, we analyzed 146 marine Salinispora and Streptomyces strains that were grown and extracted using multiple different protocols. In total, 603 samples were analyzed, generating approximately 1.8 million mass spectra. We constructed a comprehensive molecular network and identified 15 molecular families of diverse natural products and their analogues. The size and breadth of this network shows statistically supported trends in molecular diversity when comparing growth and extraction conditions. The network provides an extensive survey of the biosynthetic capacity of the strain collection and a method to compare strains based on the variety and novelty of their metabolites. This approach allows us to quickly identify patterns in metabolite production that can be linked to taxonomy, culture conditions, and extraction methods, as well as informing the most valuable growth and extraction conditions.

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“…Previous CID fragmentation studies have provided diagnostic, nominal/accurate mass information for iron (III) bound and apo (unbound) siderophores at the MS and MS 2 level and include several common ferrioxamines such as B, G, D 2 , and E (Figure 1a, b) [10][11][12][13][14]. The iron (III) unbound state is frequently more abundant in bacterial extracts and has therefore been more widely studied.…”

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confidence: 99%

Accurate Mass MS/MS/MS Analysis of Siderophores Ferrioxamine B and E1 by Collision-Induced Dissociation Electrospray Mass Spectrometry

Sidebottom

Karty

Carlson

2015

J. Am. Soc. Mass Spectrom.

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Abstract. Siderophores are bacterially secreted, small molecule iron chelators that facilitate the binding of insoluble iron (III) for reuptake and use in various biological processes. These compounds are classified by their iron (III) binding geometry, as dictated by subunit composition and include groups such as the trihydroxamates (hexadentate ligand) and catecholates (bidentate). Small modifications to the core structure such as acetylation, lipid tail addition, or cyclization, make facile characterization of new siderophores difficult by molecular ion detection alone (MS 1 ). We have expanded upon previous fragmentation-directed studies using electrospray ionization collision-induced dissociation tandem mass spectrometry (ESI-CID-MS/MS/MS) and identified diagnostic MS 3 features from the trihydroxamate siderophore class for ferrioxamine B and E1 by accurate mass. Diagnostic features for MS 3 include C-C, C-N, amide, and oxime cleavage events with proposed losses of water and -CO from the iron (III) coordination sites. These insights will facilitate the discovery of novel trihydroxamate siderophores from complex sample matrices.

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Iron acquisition in the marine actinomycete genusSalinisporais controlled by the desferrioxamine family of siderophores

Cited by 35 publications

References 53 publications

Competitive strategies differentiate closely related species of marine actinobacteria

Competitive strategies differentiate closely related species of marine actinobacteria

Prioritizing Natural Product Diversity in a Collection of 146 Bacterial Strains Based on Growth and Extraction Protocols

Accurate Mass MS/MS/MS Analysis of Siderophores Ferrioxamine B and E1 by Collision-Induced Dissociation Electrospray Mass Spectrometry

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