Development, Antibiotic Production, and Ribosome Assembly in Streptomyces venezuelae Are Impacted by RNase J and RNase III Deletion

Jones, Stephanie E.; Leong, Vivian; Elliot, Marie A.

doi:10.1128/jb.02205-14

Cited by 21 publications

(20 citation statements)

References 95 publications

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“…The rapid degradation of ribosomes in hpf null mutants has not been reported. The degradation of S. aureus ribosomes likely involves RNase III and RNase J1/J2 ( 44 ), as implicated by the accumulation of 100S dimers in Streptomyces rnc and rnj mutants ( 45 ). Curiously, decay of the GFP-tagged E. coli ribosome is not aggravated in rmf Ec and hpf Ec mutants.…”

Section: Discussionmentioning

confidence: 99%

Ribosome hibernation factor promotesStaphylococcalsurvival and differentially represses translation

2016

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In opportunistic Gram-positive Staphylococcus aureus, a small protein called hibernation-promoting factor (HPFSa) is sufficient to dimerize 2.5-MDa 70S ribosomes into a translationally inactive 100S complex. Although the 100S dimer is observed in only the stationary phase in Gram-negative gammaproteobacteria, it is ubiquitous throughout all growth phases in S. aureus. The biological significance of the 100S ribosome is poorly understood. Here, we reveal an important role of HPFSa in preserving ribosome integrity and poising cells for translational restart, a process that has significant clinical implications for relapsed staphylococcal infections. We found that the hpf null strain is severely impaired in long-term viability concomitant with a dramatic loss of intact ribosomes. Genome-wide ribosome profiling shows that eliminating HPFSa drastically increased ribosome occupancy at the 5′ end of specific mRNAs under nutrient-limited conditions, suggesting that HPFSa may suppress translation initiation. The protective function of HPFSa on ribosomes resides at the N-terminal conserved basic residues and the extended C-terminal segment, which are critical for dimerization and ribosome binding, respectively. These data provide significant insight into the functional consequences of 100S ribosome loss for protein synthesis and stress adaptation.

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Section: Discussionmentioning

confidence: 99%

Ribosome hibernation factor promotesStaphylococcalsurvival and differentially represses translation

2016

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“…RNA was isolated as described previously (43) from two replicates each of wild-type and Δ sven_4759 Δsven_5151 S. venezuelae exploring colonies grown for 8 days on YP agar plates.…”

Section: Methodsmentioning

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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“…SCO5707 is a small conserved hypothetical protein that shares homology with rimP (encoding 30S ribosomal subunit maturation factor), infB (encoding translation initiation factor IF-2), rbfA, and truB, suggesting a possible role in protein synthesis. Although transcription of the hpf gene that encodes a ribosome hibernation promoting factor (HPF) involved in 70S ribosome dimerization (45,46) is not wblC dependent ( Table 2), enrichment of HPF in the tetracycline-treated ribosome fractions suggests that translation-inactive ribosome dimers could be formed during antibiotic stress.…”

Section: Category (No Of Genes) Amentioning

confidence: 99%

The WblC/WhiB7 Transcription Factor Controls Intrinsic Resistance to Translation-Targeting Antibiotics by Altering Ribosome Composition

Lee

Yoo

Kim

et al. 2020

mBio

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Bacteria that encounter antibiotics can efficiently change their physiology to develop resistance. This intrinsic antibiotic resistance is mediated by multiple pathways, including a regulatory system(s) that activates specific genes. In some Streptomyces and Mycobacterium spp., the WblC/WhiB7 transcription factor is required for intrinsic resistance to translation-targeting antibiotics. Wide conservation of WblC/WhiB7 within Actinobacteria indicates a critical role of WblC/WhiB7 in developing resistance to such antibiotics. Here, we identified 312 WblC target genes in Streptomyces coelicolor, a model antibiotic-producing bacterium, using a combined analysis of RNA sequencing and chromatin immunoprecipitation sequencing. Interestingly, WblC controls many genes involved in translation, in addition to previously identified antibiotic resistance genes. Moreover, WblC promotes translation rate during antibiotic stress by altering the ribosome-associated protein composition. Our genome-wide analyses highlight a previously unappreciated antibiotic resistance mechanism that modifies ribosome composition and maintains the translation rate in the presence of sub-MIC levels of antibiotics. IMPORTANCE The emergence of antibiotic-resistant bacteria is one of the top threats in human health. Therefore, we need to understand how bacteria acquire resistance to antibiotics and continue growth even in the presence of antibiotics. Streptomyces coelicolor, an antibiotic-producing soil bacterium, intrinsically develops resistance to translation-targeting antibiotics. Intrinsic resistance is controlled by the WblC/WhiB7 transcription factor that is highly conserved within Actinobacteria, including Mycobacterium tuberculosis. Here, identification of the WblC/WhiB7 regulon revealed that WblC/WhiB7 controls ribosome maintenance genes and promotes translation in the presence of antibiotics by altering the composition of ribosome-associated proteins. Also, the WblC-mediated ribosomal alteration is indeed required for resistance to translation-targeting antibiotics. This suggests that inactivation of the WblC/WhiB7 regulon could be a potential target to treat antibiotic-resistant mycobacteria.

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Development, Antibiotic Production, and Ribosome Assembly in Streptomyces venezuelae Are Impacted by RNase J and RNase III Deletion

Cited by 21 publications

References 95 publications

Ribosome hibernation factor promotesStaphylococcalsurvival and differentially represses translation

Ribosome hibernation factor promotesStaphylococcalsurvival and differentially represses translation

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

The WblC/WhiB7 Transcription Factor Controls Intrinsic Resistance to Translation-Targeting Antibiotics by Altering Ribosome Composition

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