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Review
. 2016 Nov 30:5:2795.
doi: 10.12688/f1000research.9534.1. eCollection 2016.

Recent advances in understanding Streptomyces

Affiliations
Review

Recent advances in understanding Streptomyces

Keith F Chater. F1000Res. .

Abstract

About 2,500 papers dated 2014-2016 were recovered by searching the PubMed database for Streptomyces, which are the richest known source of antibiotics. This review integrates around 100 of these papers in sections dealing with evolution, ecology, pathogenicity, growth and development, stress responses and secondary metabolism, gene expression, and technical advances. Genomic approaches have greatly accelerated progress. For example, it has been definitively shown that interspecies recombination of conserved genes has occurred during evolution, in addition to exchanges of some of the tens of thousands of non-conserved accessory genes. The closeness of the association of Streptomyces with plants, fungi, and insects has become clear and is reflected in the importance of regulators of cellulose and chitin utilisation in overall Streptomyces biology. Interestingly, endogenous cellulose-like glycans are also proving important in hyphal growth and in the clumping that affects industrial fermentations. Nucleotide secondary messengers, including cyclic di-GMP, have been shown to provide key input into developmental processes such as germination and reproductive growth, while late morphological changes during sporulation involve control by phosphorylation. The discovery that nitric oxide is produced endogenously puts a new face on speculative models in which regulatory Wbl proteins (peculiar to actinobacteria) respond to nitric oxide produced in stressful physiological transitions. Some dramatic insights have come from a new model system for Streptomyces developmental biology, Streptomyces venezuelae, including molecular evidence of very close interplay in each of two pairs of regulatory proteins. An extra dimension has been added to the many complexities of the regulation of secondary metabolism by findings of regulatory crosstalk within and between pathways, and even between species, mediated by end products. Among many outcomes from the application of chromosome immunoprecipitation sequencing (ChIP-seq) analysis and other methods based on "next-generation sequencing" has been the finding that 21% of Streptomyces mRNA species lack leader sequences and conventional ribosome binding sites. Further technical advances now emerging should lead to continued acceleration of knowledge, and more effective exploitation, of these astonishing and critically important organisms.

Keywords: genomics; pathogenic streptomyces; streptomyces; streptomyces ecology; streptomyces evolution.

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Conflict of interest statement

The author declares that he has no competing interests. No competing interests were disclosed. No competing interests were disclosed. No competing interests were disclosed. No competing interests were disclosed.

Figures

Figure 1.
Figure 1.. Colonies of Streptomyces coelicolor A3(2).
The fuzzy surface of these mould-like colonies is made up of aerial hyphae carrying chains of spores (photo, K.F. Chater).
Figure 2.
Figure 2.. Recent discoveries about germination and hyphal growth.
Three different nucleotide signalling molecules are involved in stimulating the production of peptidoglycan hydrolase(s) (Rpf, for resuscitation-promoting factors), leading to remodelling of the spore wall and the emergence of a germ tube . Continued hyphal elongation is co-ordinated by the DivIVA-based polarisome and (in addition to cell wall growth) involves the extracellular production of cellulose-like glycan catalysed by polarisome-linked ClsA (cellulose synthase-like) associated with the copper oxidase GlxA , . MatAB proteins have an uncharacterised role in glycan production . Vesicular membrane structures form in apparently irregular locations within hyphae, and some of them extend across the hyphal compartment, separating nucleoids , .
Figure 3.
Figure 3.. Model integrating the nitrogen oxide cycle (ochre) with mycothiol cycling (yellow) and with morphological development mediated by Wbl proteins (red) in Streptomyces coelicolor.
In the nitrogen oxide cycle , nitrate generated intracellularly by an unknown pathway is reduced to nitrite mainly by the NarG2 enzyme . Nitrite is the source of nitric oxide (NO) (mechanism unknown) . Nitric oxide is oxidised to nitrate by flavohaemoglobins specified by SCO7428 (incorrectly given as SCO7472 in 84) and SCO7094, which are induced when nitric oxide binds to NsrR, the repressor of both genes , . Internal nitric oxide also binds the haem-containing sensor kinase DevS, which then phosphorylates the cognate response regulator DevR. DevR-P induces Nar2 in an autoinducing feedforward loop . Nitric oxide binds strongly to Wbl proteins such as WblA, WhiB, and WhiD, modulating their regulatory activity and hence coordinating differentiation. Other regulatory components may take part in the action of Wbl proteins: for example, WhiB target genes are all also dependent on WhiA protein . It is speculated that the Wbl proteins are denitrosylated by the SCO4179 (nitrobindin?)-mediated transfer of nitric oxide to mycothiol (MSH) to generate MSNO . MSNO is denitrosylated by MSNO reductase, with the resulting oxidised mycothiol then being reduced to MSH by an undetermined mechanism.
Figure 4.
Figure 4.. Schematic diagram of recent discoveries about late stages in sporulation.
As aerial hyphae approach sporulation, c-di-GMP phosphodiesterase releases ftsZ from repression by BldD:c-di-GMP , , . FtsZ attaches to SsgB, held at regularly spaced positions by membrane-bound SepG . Another SsgB-like protein, SsgA, also plays a role in SsgB location, which is less well defined . FtsZ then condenses into Z-rings, which guide septation, and SepG relocates to the periphery of the prespore compartments . The spore wall remodelling complex, held in an inactive phosphorylated state, is activated by one or more of many phosphorylases and, apparently with the involvement of SepG, causes prespores to become rounder and thicker walled. I tentatively suggest that the increased amounts of SepG at this stage may depend on the Wbl-type regulator WhiD (possibly influenced by nitric oxide [NO] – see Figure 3), since sepG and whiD null mutants have very similar phenotypes , .

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References

    1. Charlop-Powers Z, Owen JG, Reddy BV, et al. : Chemical-biogeographic survey of secondary metabolism in soil. Proc Natl Acad Sci U S A. 2014;111(10):3757–62. 10.1073/pnas.1318021111 - DOI - PMC - PubMed
    1. Charlop-Powers Z, Owen JG, Reddy BV, et al. : Global biogeographic sampling of bacterial secondary metabolism. eLife. 2015;4:e05048. 10.7554/eLife.05048 - DOI - PMC - PubMed
    1. Hopwood DA: Streptomyces in Nature and Medicine: The Antibiotic Makers. Oxford University Press, New York, NY.2007. 10.1093/jhmas/jrn016 - DOI
    1. Chater KF, Biró S, Lee KJ, et al. : The complex extracellular biology of Streptomyces. FEMS Microbiol Rev. 2010;34(2):171–98. 10.1111/j.1574-6976.2009.00206.x - DOI - PubMed
    1. Wibberg D, Al-Dilaimi A, Busche T, et al. : Complete genome sequence of Streptomyces reticuli, an efficient degrader of crystalline cellulose. J Biotechnol. 2016;222:13–4. 10.1016/j.jbiotec.2016.02.002 - DOI - PubMed

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The authors declared that no grants were involved in supporting this work.

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