‘Exploring’ the regulation of Streptomyces growth and development

Jones, Stephanie E.; Elliot, Marie A.

doi:10.1016/j.mib.2017.09.009

Cited by 34 publications

(23 citation statements)

References 39 publications

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“…In soil, these bacteria are best known for their ability to produce a vast array of specialized metabolites and for their complex, filamentous life cycle (8, 9). Recent work has, however, revealed that Streptomyces species also use volatile compounds to promote an alternative growth strategy known as “exploration” (10, 11). In the model species Streptomyces venezuelae, exploration is initiated in response to the production of the VOC trimethylamine (TMA), which promotes the rapid spreading of explorer cells across surfaces.…”

Section: Introductionmentioning

confidence: 99%

StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

Jones

Pham

Zambri

et al. 2019

mBio

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Bacteria and fungi produce a wide array of volatile organic compounds (VOCs), and these can act as chemical cues or as competitive tools. Recent work has shown that the VOC trimethylamine (TMA) can promote a new form of Streptomyces growth, termed “exploration.” Here, we report that TMA also serves to alter nutrient availability in the area surrounding exploring cultures: TMA dramatically increases the environmental pH and, in doing so, reduces iron availability. This, in turn, compromises the growth of other soil bacteria and fungi. In response to this low-iron environment, Streptomyces venezuelae secretes a suite of differentially modified siderophores and upregulates genes associated with siderophore uptake. Further reducing iron levels by limiting siderophore uptake or growing cultures in the presence of iron chelators enhanced exploration. Exploration was also increased when S. venezuelae was grown in association with the related low-iron- and TMA-tolerant Amycolatopsis bacteria, due to competition for available iron. We are only beginning to appreciate the role of VOCs in natural communities. This work reveals a new role for VOCs in modulating iron levels in the environment and implies a critical role for VOCs in modulating the behavior of microbes and the makeup of their communities. It further adds a new dimension to our understanding of the interspecies interactions that influence Streptomyces exploration and highlights the importance of iron in exploration modulation. IMPORTANCE Microbial growth and community interactions are influenced by a multitude of factors. A new mode of Streptomyces growth—exploration—is promoted by interactions with the yeast Saccharomyces cerevisiae and requires the emission of trimethylamine (TMA), a pH-raising volatile compound. We show here that TMA emission also profoundly alters the environment around exploring cultures. It specifically reduces iron availability, and this in turn adversely affects the viability of surrounding microbes. Paradoxically, Streptomyces bacteria thrive in these iron-depleted niches, both rewiring their gene expression and metabolism to facilitate iron uptake and increasing their exploration rate. Growth in close proximity to other microbes adept at iron uptake also enhances exploration. Collectively, the data from this work reveal a new role for bacterial volatile compounds in modulating nutrient availability and microbial community behavior. The results further expand the repertoire of interspecies interactions and nutrient cues that impact Streptomyces exploration and provide new mechanistic insight into this unique mode of bacterial growth.

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Section: Introductionmentioning

confidence: 99%

StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

Jones

Pham

Zambri

et al. 2019

mBio

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“…). Recently, a distinct ‘exploratory’ growth mode has been identified in which non‐branching vegetative hyphae of Streptomyces rapidly extend across surfaces, in response to glucose starvation and the presence of a volatile compound, trimethylamine, that raises pH (Jones et al , ; Jones and Elliot, ). However, S. venezuelae mutants lacking the Wbls WhiB or WhiD are still competent to explore, showing that they do not regulate this process (Jones et al , ).…”

Section: Introductionmentioning

confidence: 99%

The actinobacterial WhiB‐like (Wbl) family of transcription factors

Bush

2018

Molecular Microbiology

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SummaryThe WhiB‐like (Wbl) family of proteins are exclusively found in Actinobacteria. Wbls have been shown to play key roles in virulence and antibiotic resistance in Mycobacteria and Corynebacteria, reflecting their importance during infection by the human pathogens Mycobacterium tuberculosis, Mycobacterium leprae and Corynebacterium diphtheriae. In the antibiotic‐producing Streptomyces, several Wbls have important roles in the regulation of morphological differentiation, including WhiB, a protein that controls the initiation of sporulation septation and the founding member of the Wbl family. In recent years, genome sequencing has revealed the prevalence of Wbl paralogues in species throughout the Actinobacteria. Wbl proteins are small (generally ~80–140 residues) and each contains four invariant cysteine residues that bind an O2‐ and NO‐sensitive [4Fe–4S] cluster, raising the question as to how they can maintain distinct cellular functions within a given species. Despite their discovery over 25 years ago, the Wbl protein family has largely remained enigmatic. Here I summarise recent research in Mycobacteria, Corynebacteria and Streptomyces that sheds light on the biochemical function of Wbls as transcription factors and as potential sensors of O2 and NO. I suggest that Wbl evolution has created diversity in protein–protein interactions, [4Fe–4S] cluster‐sensitivity and the ability to bind DNA.

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“…become limiting, it produces hydrophobic aerial hyphae that develop into chains of dispersible spores (4,5). The spores are less robust than endospores of firmicutes, but they nevertheless confer upon the bacterium a considerable survival advantage under adverse conditions.…”

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confidence: 99%

Activity of Spore-Specific Respiratory Nitrate Reductase 1 of Streptomyces coelicolor A3(2) Requires a Functional Cytochrome bcc-aa ₃ Oxidase Supercomplex

et al. 2019

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Spores have strongly reduced metabolic activity and are produced during the complex developmental cycle of the actinobacteriumStreptomyces coelicolor. Resting spores can remain viable for decades, yet little is known about how they conserve energy. It is known, however, that they can reduce either oxygen or nitrate using endogenous electron sources.S. coelicoloruses either a cytochromebdoxidase or a cytochromebcc-aa3oxidase supercomplex to reduce oxygen, while nitrate is reduced by Nar-type nitrate reductases, which typically oxidize quinol directly. Here, we show that in resting spores the Nar1 nitrate reductase requires a functionalbcc-aa3supercomplex to reduce nitrate. Mutants lacking the completeqcr-ctagenetic locus encoding thebcc-aa3supercomplex showed no Nar1-dependent nitrate reduction. Recovery of Nar1 activity was achieved by genetic complementation but only when the completeqcr-ctalocus was reintroduced to the mutant strain. We could exclude that the dependence on the supercomplex for nitrate reduction was via regulation of nitrate transport. Moreover, the catalytic subunit, NarG1, of Nar1 was synthesized in theqcr-ctamutant, ruling out transcriptional control. Constitutive synthesis of Nar1 in mycelium revealed that the enzyme was poorly active in this compartment, suggesting that the Nar1 enzyme cannot act as a typical quinol oxidase. Notably, nitrate reduction by the Nar2 enzyme, which is active in growing mycelium, was not wholly dependent on thebcc-aa3supercomplex for activity. Together, our data suggest that Nar1 functions together with the proton-translocatingbcc-aa3supercomplex to increase the efficiency of energy conservation in resting spores.IMPORTANCEStreptomyces coelicolorforms spores that respire with either oxygen or nitrate, using only endogenous electron donors. This helps maintain a membrane potential and, thus, viability. Respiratory nitrate reductase (Nar) usually receives electrons directly from reduced quinone species; however, we show that nitrate respiration in spores requires a respiratory supercomplex comprising cytochromebccoxidoreductase andaa3oxidase. Our findings suggest that the Nar1 enzyme in theS. coelicolorspore functions together with the proton-translocatingbcc-aa3supercomplex to help maintain the membrane potential more efficiently. Dissecting the mechanisms underlying this survival strategy is important for our general understanding of bacterial persistence during infection processes and of how bacteria might deal with nutrient limitation in the natural environment.

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‘Exploring’ the regulation of Streptomyces growth and development

Cited by 34 publications

References 39 publications

StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

The actinobacterial WhiB‐like (Wbl) family of transcription factors

Activity of Spore-Specific Respiratory Nitrate Reductase 1 of Streptomyces coelicolor A3(2) Requires a Functional Cytochrome bcc-aa ₃ Oxidase Supercomplex

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‘Exploring’ the regulation of Streptomyces growth and development

Cited by 34 publications

References 39 publications

StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

StreptomycesVolatile Compounds Influence Exploration and Microbial Community Dynamics by Altering Iron Availability

The actinobacterial WhiB‐like (Wbl) family of transcription factors

Activity of Spore-Specific Respiratory Nitrate Reductase 1 of Streptomyces coelicolor A3(2) Requires a Functional Cytochrome bcc-aa 3 Oxidase Supercomplex

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Activity of Spore-Specific Respiratory Nitrate Reductase 1 of Streptomyces coelicolor A3(2) Requires a Functional Cytochrome bcc-aa ₃ Oxidase Supercomplex