Uptake of xenosiderophores in <i>Bacillus subtilis</i> occurs with high affinity and enhances the folding stabilities of substrate binding proteins

Miethke, Marcus; Kraushaar, Timo; Marahiel, Mohamed A.

doi:10.1016/j.febslet.2012.11.027

Cited by 29 publications

(27 citation statements)

References 42 publications

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“…Instead, P. fluorescens very likely utilizes the S. ambofaciens siderophores desferrioxamine B and coelichelin as xenosiderophores, thanks to its FoxA receptor. In contrast to most studies, in which the use of xenosiderophores was revealed indirectly through the addition of purified siderophore to the growth medium (44)(45)(46)(47), binding affinity assays (11,48), or native PAGE and surface plasmon resonance (49) or with labeled iron (11,50,51), we revealed potential iron piracy through a direct interaction between a Gram-positive and a Gram-negative bacterium. This potential piracy likely occurs only in one direction.…”

Section: Discussioncontrasting

confidence: 91%

Pseudomonas fluorescens Pirates both Ferrioxamine and Ferricoelichelin Siderophores from Streptomyces ambofaciens

Galet

Deveau

Hôtel

et al. 2015

Appl Environ Microbiol

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Iron is essential in many biological processes. However, its bioavailability is reduced in aerobic environments, such as soil. To overcome this limitation, microorganisms have developed different strategies, such as iron chelation by siderophores. Some bacteria have even gained the ability to detect and utilize xenosiderophores, i.e., siderophores produced by other organisms. We illustrate an example of such an interaction between two soil bacteria, Pseudomonas fluorescens strain BBc6R8 and Streptomyces ambofaciens ATCC 23877, which produce the siderophores pyoverdine and enantiopyochelin and the siderophores desferrioxamines B and E and coelichelin, respectively. During pairwise cultures on iron-limiting agar medium, no induction of siderophore synthesis by P. fluorescens BBc6R8 was observed in the presence of S. ambofaciens ATCC 23877. Cocultures with a Streptomyces mutant strain that produced either coelichelin or desferrioxamines, as well as culture in a medium supplemented with desferrioxamine B, resulted in the absence of pyoverdine production; however, culture with a double mutant deficient in desferrioxamines and coelichelin production did not. This strongly suggests that P. fluorescens BBbc6R8 utilizes the ferrioxamines and ferricoelichelin produced by S. ambofaciens as xenosiderophores and therefore no longer activates the production of its own siderophores. A screening of a library of P. fluorescens BBc6R8 mutants highlighted the involvement of the TonB-dependent receptor FoxA in this process: the expression of foxA and genes involved in the regulation of its biosynthesis was induced in the presence of S. ambofaciens. In a competitive environment, such as soil, siderophore piracy could well be one of the driving forces that determine the outcome of microbial competition. Bacteria detect, assimilate, and integrate different environmental signals in order to better adapt to their habitat and cope with changes in environmental conditions. Multiple signaling pathways allow them to communicate with each other within the same species or between different species (1). This can be achieved through the production and detection of diffusible molecules in the environment. In response to these interactions, the microorganisms have developed complex metabolic and physiological responses. One of the essential environmental factors vital for organisms is iron. It plays an essential role in many biological processes, such as DNA synthesis, respiration, and photosynthesis. Iron can adopt two different ionic forms, Fe 2ϩ and Fe 3ϩ . This property makes it an important player in the oxidation-reduction reactions in the cell. However, while iron is an abundant element on earth, its bioavailability is reduced in aerobic environments, such as soil. Ferric iron (Fe 3ϩ ) forms insoluble ferric hydroxides (with a solubility product of ϳ10 Ϫ39 ) in the presence of oxygen (2-4). Therefore, iron is a limiting factor for the growth of microorganisms.To overcome the limitation of iron bioavailability, aerobic bacteria have develop...

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Section: Discussioncontrasting

confidence: 91%

Pseudomonas fluorescens Pirates both Ferrioxamine and Ferricoelichelin Siderophores from Streptomyces ambofaciens

Galet

Deveau

Hôtel

et al. 2015

Appl Environ Microbiol

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“…subtilis has six siderophore-specific SBPs (28). These proteins are tethered to the outside of cells, where they bind iron-bound siderophores for uptake into the cells through ABC-type transporters.…”

Section: Resultsmentioning

confidence: 99%

“…subtilis is able to pirate multiple classes of siderophores using its diverse range of siderophore uptake systems (28). To determine whether promotion of sporulation gene expression was specific to enterobactin or was a general response to xenosiderophores, we tested the activities of multiple siderophores in our microcolony lawn assay.…”

Section: Resultsmentioning

confidence: 99%

“…coli may be biologically relevant, as the environmental niches of these two bacteria overlap. In addition, we have shown that ferrichrome (produced by multiple fungi [28, 57]) and ferrioxamine E (produced by streptomycetes [28, 58]) also promote sporulation in B. subtilis.…”

Section: Discussionmentioning

confidence: 99%

“…In addition to making bacillibactin, B. subtilis has the ability to pirate a range of xenosiderophores, including enterobactin (28, 31, 32). The B.…”

Section: Introductionmentioning

confidence: 99%

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Pirated Siderophores Promote Sporulation in Bacillus subtilis

Grandchamp

Caro

Shank

2017

Appl Environ Microbiol

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In microbial communities, bacteria chemically and physically interact with one another. Some of these interactions are mediated by secreted specialized metabolites that act as either intraspecies or interspecies signals to alter gene expression and to change cell physiology. Bacillus subtilis is a well-characterized soil microbe that can differentiate into multiple cell types, including metabolically dormant endospores. We were interested in identifying microbial interactions that affected sporulation in B. subtilis. Using a fluorescent transcriptional reporter, we observed that coculturing B. subtilis with Escherichia coli promoted sporulation gene expression via a secreted metabolite. To identify the active compound, we screened the E. coli Keio Collection and identified the sporulation-accelerating cue as the siderophore enterobactin. B. subtilis has multiple iron acquisition systems that are used to take up the B. subtilis-produced siderophore bacillibactin, as well as to pirate exogenous siderophores such as enterobactin. While B. subtilis uses a single substrate binding protein (FeuA) to take up both bacillibactin and enterobactin, we discovered that it requires two distinct genes to sporulate in response to these siderophores (the esterase gene besA for bacillibactin and a putative esterase gene, ybbA, for enterobactin). In addition, we found that siderophores from a variety of other microbial species also promote sporulation in B. subtilis. Our results thus demonstrate that siderophores can act not only as bacterial iron acquisition systems but also as interspecies cues that alter cellular development and accelerate sporulation in B. subtilis.IMPORTANCE While much is known about the genetic regulation of Bacillus subtilis sporulation, little is understood about how other bacteria influence this process. This work describes an interaction between Escherichia coli and B. subtilis that accelerates sporulation in B. subtilis. The interaction is mediated by the E. coli siderophore enterobactin; we show that other species' siderophores also promote sporulation gene expression in B. subtilis. These results suggest that siderophores not only may supply bacteria with the mineral nutrient iron but also may play a role in bacterial interspecies signaling, providing a cue for sporulation. Siderophores are produced by many bacterial species and thus potentially play important roles in altering bacterial cell physiology in diverse environments.

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Carbon Cycle Implications of Soil Microbial Interactions

Ramin

Allison

2019

Advances in Environmental Microbiology

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The soil environment contains the largest pool of carbon on Earth, with controls on soil carbon residency and flux being an emergent property of microbial metabolism. Despite the fact that microbial interactions have metabolic implications, the contribution of interactions are often overlooked regarding the carbon cycle. Here, we hypothesize that microbial interactions are intrinsically coupled to carbon cycling through eco-evolutionary principles. Interactions drive phenotypic responses that result in allocation pattern shifts and changes in carbon use efficiency. These changes promote alterations in resource availability and community structure, thereby creating selective pressures that contribute to diffuse evolutionary mechanisms. The outcomes then feed back into microbial metabolic operations with consequences for carbon turnover, continuing a feedback loop of microbial interactions, evolutionary processes, and the carbon cycle.

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Uptake of xenosiderophores in Bacillus subtilis occurs with high affinity and enhances the folding stabilities of substrate binding proteins

Cited by 29 publications

References 42 publications

Pseudomonas fluorescens Pirates both Ferrioxamine and Ferricoelichelin Siderophores from Streptomyces ambofaciens

Pseudomonas fluorescens Pirates both Ferrioxamine and Ferricoelichelin Siderophores from Streptomyces ambofaciens

Pirated Siderophores Promote Sporulation in Bacillus subtilis

Carbon Cycle Implications of Soil Microbial Interactions

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