A Waking Review: Old and Novel Insights into the Spore Germination in Streptomyces

Bobek, Jan; Šmídová, Klára; Čihák, Matouš

doi:10.3389/fmicb.2017.02205

Cited by 52 publications

(54 citation statements)

References 166 publications

(225 reference statements)

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“…A good survival strategy of some bacteria and fungi is the latency stage of spores. Under this stage, cells stop growing and their metabolism is mainly inactive [2]. Spores are very resistant to stress conditions.…”

Section: Solid Culturesmentioning

confidence: 99%

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Streptomyces as a Source of Antimicrobials: Novel Approaches to Activate Cryptic Secondary Metabolite Pathways

Manteca¹,

Yagüe²

2019

Antimicrobials, Antibiotic Resistance, Antibiofilm Strategies and Activity Methods

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Streptomyces is the most important bacterial genus for bioactive compound production. These soil bacteria are characterized by a complex differentiation cycle. Streptomyces is extremely important in biotechnology, producing approximately two thirds of all antibiotics, as well as many compounds of medical and agricultural interest. Drug discovery from streptomycetes became challenging once the most common compounds were discovered, and the system was basically abandoned by industry. Simultaneously, antibiotic resistance is increasing dramatically, and new antibiotics are required. Screening from nature is being resumed (exploring new environments, looking for elicitors, metagenome, etc.). Secondary metabolism is conditioned by differentiation; although the relationship between both has long remained elusive, differentiation as a trigger for antibiotic production remains basically unexplored. Most cultures used in screening campaigns for new bioactive molecules have been performed empirically, and workflow was extremely productive during the so-called golden age of antibiotics; however, currently there is a bottleneck. Streptomyces is still the most important natural source of antibiotics, and it also harbors many cryptic secondary metabolite pathways not expressed under laboratory conditions. In this chapter, we review strategies based on differentiation, one of the keys improving secondary metabolite production and activating cryptic pathways to face the challenges of drug discovery.

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Section: Solid Culturesmentioning

confidence: 99%

“…In this dehydrated environment, molecules have inactive conformations (denaturalized proteins, etc.) that are stabilized and protected by the sugar trehalose [2]. From this null or limited metabolism, spores are able to germinate, as the macromolecules needed have already been synthesized before the latency stage [2].…”

Section: Solid Culturesmentioning

confidence: 99%

Streptomyces as a Source of Antimicrobials: Novel Approaches to Activate Cryptic Secondary Metabolite Pathways

Manteca¹,

Yagüe²

2019

Antimicrobials, Antibiotic Resistance, Antibiofilm Strategies and Activity Methods

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“…We focused on the Streptomyces because they are ubiquitous saprophytes and have complicated life cycles consisting of germination, mycelial growth (with doubling times of 2–3 hr on rich media) and sporulation (Hopwood, Kieser, Bibb, Buttner, & Chater, ). The impact of life cycle stages on the distribution of descendants is particularly poorly understood (Bobek, Šmídová, & Čihák, ). Using the variability between replicates, we show that the distribution of descendants is heavy‐tailed—that is some bacteria represent a far greater proportion of the final population than their initial frequency.…”

Section: Introductionmentioning

confidence: 99%

Stochastic exits from dormancy give rise to heavy‐tailed distributions of descendants in bacterial populations

Wright

Vetsigian

2019

Molecular Ecology

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Variance in reproductive success is a major determinant of the degree of genetic drift in a population. While many plants and animals exhibit high variance in their number of progeny, far less is known about these distributions for microorganisms. Here, we used a strain barcoding approach to quantify variability in offspring number among replicate bacterial populations and developed a Bayesian method to infer the distribution of descendants from this variability. We applied our approach to measure the offspring distributions for five strains of bacteria from the genus Streptomyces after germination and growth in a homogenous laboratory environment. The distributions of descendants were heavy‐tailed, with a few cells effectively ‘winning the jackpot’ to become a disproportionately large fraction of the population. This extreme variability in reproductive success largely traced back to initial populations of spores stochastically exiting dormancy, which provided early‐germinating spores with an exponential advantage. In simulations with multiple dormancy cycles, heavy‐tailed distributions of descendants decreased the effective population size by many orders of magnitude and led to allele dynamics differing substantially from classical population genetics models with matching effective population size. Collectively, these results demonstrate that extreme variability in reproductive success can occur even in growth conditions that are far more homogeneous than the natural environment. Thus, extreme variability in reproductive success might be an important factor shaping microbial population dynamics with implications for predicting the fate of beneficial mutations, interpreting sequence variability within populations and explaining variability in infection outcomes across patients.

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“…This microorganism was isolated from South American soil samples and first described by Higgens and Kastner (). In addition to other members of the Streptomyces genus, it exhibits a very complex life cycle that includes multicellular, spore‐bearing hyphae and semi‐dormant spores that can survive for long periods in the soil (Bobek, Šmídová, & Čihák, ). Moreover, it was described that S. clavuligerus produces more than 20 secondary metabolites, including cephamycin C, holomycin, deacetoxycephalosporin C, penicillin N, and tunicamycin, among others (Table ).…”

Section: Introductionmentioning

confidence: 99%

A putative antimicrobial peptide from Hymenoptera in the megaplasmid pSCL4 of Streptomyces clavuligerus ATCC 27064 reveals a singular case of horizontal gene transfer with potential applications

Ayala-Ruano

Santander-Gordón

Tejera

et al. 2019

Ecology and Evolution

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Streptomyces clavuligerus is a Gram‐positive bacterium that is a high producer of secondary metabolites with industrial applications. The production of antibiotics such as clavulanic acid or cephamycin has been extensively studied in this species; nevertheless, other aspects, such as evolution or ecology, have received less attention. Furthermore, genes that arise from ancient events of lateral transfer have been demonstrated to be implicated in important functions of host species. This approximation discovered relevant genes that genomic analyses overlooked. Thus, we studied the impact of horizontal gene transfer in the S. clavuligerus genome. To perform this task, we applied whole‐genome analysis to identify a laterally transferred sequence from different domains. The most relevant result was a putative antimicrobial peptide (AMP) with a clear origin in the Hymenoptera order of insects. Next, we determined that two copies of these genes were present in the megaplasmid pSCL4 but absent in the S. clavuligerus ATCC 27064 chromosome. Additionally, we found that these sequences were exclusive to the ATCC 27064 strain (and so were not present in any other bacteria) and we also verified the expression of the genes using RNAseq data. Next, we used several AMP predictors to validate the original annotation extracted from Hymenoptera sequences and explored the possibility that these proteins had post‐translational modifications using peptidase cleavage prediction. We suggest that Hymenoptera AMP‐like proteins of S. clavuligerus ATCC 27064 may be useful for both species adaptation and as an antimicrobial molecule with industrial applications.

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A Waking Review: Old and Novel Insights into the Spore Germination in Streptomyces

Cited by 52 publications

References 166 publications

Streptomyces as a Source of Antimicrobials: Novel Approaches to Activate Cryptic Secondary Metabolite Pathways

Streptomyces as a Source of Antimicrobials: Novel Approaches to Activate Cryptic Secondary Metabolite Pathways

Stochastic exits from dormancy give rise to heavy‐tailed distributions of descendants in bacterial populations

A putative antimicrobial peptide from Hymenoptera in the megaplasmid pSCL4 of Streptomyces clavuligerus ATCC 27064 reveals a singular case of horizontal gene transfer with potential applications

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