How Streptomyces thrive: Advancing our understanding of classical development and uncovering new behaviors

Zambri, Matthew; Williams, Michelle A.; Elliot, Marie A.

doi:10.1016/bs.ampbs.2022.01.004

Cited by 8 publications

(7 citation statements)

References 128 publications

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“…The copyright holder for this preprint this version posted January 13, 2023. ; https://doi.org/10.1101/2023.01.12.523877 doi: bioRxiv preprint response system for diverse stimuli that can be derived from environment including bacterial interaction (16), what we have observed so far for morphological behavior would be only a limited fraction and large parts are remain unrevealed.…”

Section: Streptomyces Species Have a Complex Life Cycle Unlike Other ...mentioning

confidence: 89%

“…Unique example has been known such as exploratory growth of Streptomyces species by significant polar tip extension, which is induced by alkalized condition caused by fungi (15). However, as Streptomyces species has evolved complex response system for diverse stimuli that can be derived from environment including bacterial interaction (16), what we have observed so far for morphological behavior would be only a limited fraction and large parts are remain unrevealed.…”

Section: Introductionmentioning

confidence: 93%

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Redox-active compound generated by bacterial crosstalk induces hypha branching inStreptomycesspecies

Kato

Asamizu

Onaka

2023

Preprint

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Chemical cross talks betweenMycolicibacterium septicumHEK138M andBacillus subtilis168 affect the bacterial morphology ofStreptomyces variegatusHEK138A. We found thatS. variegatusexhibits unusual hyphae branching by the bacterial interaction. We aimed to elucidate the mechanism by performing activity guided purification of substances that induce the unusual cell morphology. We found that pyrogallol, a redox active aromatic small molecule induced significant hyphae branching inS. variegatusand the activity was also observed in some of otherStreptomycesspecies. Interestingly, the pyrogallol activity was diminished by adding catalase, which broke down H2O2. To further confirm the involvement, H2O2was tested and similar activity which induced hyphal branching was observed. This indicates that reactive oxygen species (ROS) generated by redox-active compound (RAC) is the inducing factor of hyphae branching. Further investigation revealed that pyrogallol was generated by NahG enzyme homolog ofM. septicumusing 2,3-dihydroxybenzoic acid as substrate by heterologous expression inE. coli. Moreover, co-culture with gene knock-out mutants revealed that 2,3-dihydroxybenzoic acid was supplied byB. subtilisproduced as intermediate of bacterial siderophore bacillibactin. Since the hyphae branching of vegetative mycelium can increase the density of filamentous network and consequently help secure the milieu in soil, our results suggested that those filamentous soil bacteria use ROS which can be supplied from plant derived RAC as a signal. As those RAC ubiquitously exist in soil environment, the system will be beneficial for sensing the nutrient sources in addition to the generally considered defensive response to oxidative stress.

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Section: Streptomyces Species Have a Complex Life Cycle Unlike Other ...mentioning

confidence: 89%

Section: Introductionmentioning

confidence: 93%

Redox-active compound generated by bacterial crosstalk induces hypha branching inStreptomycesspecies

Kato

Asamizu

Onaka

2023

Preprint

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“…Today, up to two-thirds of all nature-based antibiotics used in the clinics are produced by Streptomyces spp 1–3 . Furthermore, the intricate life cycle of Streptomyces positions it as a model for the study of multicellular development in bacteria 4 . Microbial interaction was shown to be a prominent trigger of secondary metabolite production and cellular development.…”

Section: Introductionmentioning

confidence: 99%

“…Today, up to two-thirds of all nature-based antibiotics used in the clinics are produced by Streptomyces spp [1][2][3] . Furthermore, the intricate life cycle of Streptomyces positions it as a model for the study of multicellular development in bacteria 4 .…”

Section: Introductionmentioning

confidence: 99%

Isolation and characterization of the newStreptomycesphages Kamino, Geonosis, Abafar and Scarif infecting a broad range of host species

Rackow,

Rolland,

Mohnen

et al. 2024

Preprint

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Streptomyces, a multifaceted genus of soil-dwelling bacteria within the phylum Actinobacteria, features intricate phage-host interactions shaped by its complex life cycle and the synthesis of a diverse array of specialized metabolites. Here, we describe the isolation and characterization of four novelStreptomycesphages infecting a variety of different host species. While phage Kamino, isolated onStreptomyces kasugaensis, is predicted to be temperate and encodes a serine integrase in its genome, phages Geonosis (isolated onS. griseus) and phages Abafar and Scarif, isolated onS. albidoflavus, are virulent phages. Phages Kamino and Geonosis were shown to amplify well in liquid culture leading to a pronounced culture collapse already at low titres. Determination of the host range by testing >40 differentStreptomycesspecies identified phages Kamino, Abafar and Scarif as broad host range phages, with Kamino showing productive infections on 15 different species. Isolated phages were further tested regarding their sensitivity to antiphage molecules. Here, the strongest effects were observed for the DNA-intercalating molecule daunorubicin. Overall, the phages described in this study expand the publicly available portfolio of phages infectingStreptomycesand will be instrumental for advancing the mechanistic understanding of the intricate antiviral strategies employed by these multicellular bacteria.

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“…Beyond their impressive biosynthetic capabilities, Streptomyces have a complex multicellular, sporulating life cycle. This life cycle begins with spore germination, followed by hyphal tip extension and branching ( 8 , 9 ). The resulting vegetative mycelium continues growing until reproductive growth initiates, where reproductive growth involves raising unbranched aerial hyphae and subsequently converting these hyphal filaments into chains of dormant spores.…”

Section: Introductionmentioning

confidence: 99%

Redefining development in Streptomyces venezuelae : integrating exploration into the classical sporulating life cycle

Shepherdson,

Elliot

2024

mBio

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Two growth modes have been described for the filamentous Streptomyces bacteria. Their classic developmental life cycle culminates in the formation of dormant spores, where movement to new environments is mediated through spore dispersal. In contrast, exploratory growth proceeds as a rapidly expanding vegetative mycelium that leads to extensive surface colonization and is associated with the release of volatile compounds that promote alkalinization (and reduced iron bioavailability) of its surrounding environment. Here, we report that exploratory growth in Streptomyces venezuelae can proceed in tandem with classic sporulating development in response to specific nutritional cues. Sporulating exploration is not accompanied by a rise in environmental pH but has the same iron acquisition requirements as conventional exploration. We found that mutants that were defective in their ability to sporulate were unaffected in exploration, but mutants undergoing precocious sporulation were compromised in their exploratory growth and this appeared to be mediated through premature activation of the developmental regulator WhiI. Cell envelope integrity was also found to be critical for exploration, as mutations in the cell envelope stress-responsive extracytoplasmic function sigma factor SigE led to a failure to explore robustly under all exploration-promoting conditions. Finally, in expanding the known exploration-promoting conditions, we discovered that the model species Streptomyces lividans exhibited exploration capabilities, supporting the proposal that exploration is conserved across diverse streptomycetes. IMPORTANCE Streptomyces bacteria have evolved diverse developmental and metabolic strategies to thrive in dynamic environmental niches. Here, we report the amalgamation of previously disparate developmental pathways, showing that colony expansion via exploration can proceed in tandem with colony sporulation. This developmental integration extends beyond phenotype to include shared genetic elements, with sporulation-specific repressors being required for successful exploration. Comparing this new exploration mode with previously identified strategies has revealed key differences (e.g., no need for environmental alkalinization), and simultaneously allowed us to define unifying requirements for Streptomyces exploration. The “reproductive exploration” phenomenon reported here represents a unique bet-hedging strategy, with the Streptomyces colony engaging in an aggressive colonization strategy while transporting a protected genetic repository.

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How Streptomyces thrive: Advancing our understanding of classical development and uncovering new behaviors

Cited by 8 publications

References 128 publications

Redox-active compound generated by bacterial crosstalk induces hypha branching inStreptomycesspecies

Redox-active compound generated by bacterial crosstalk induces hypha branching inStreptomycesspecies

Isolation and characterization of the newStreptomycesphages Kamino, Geonosis, Abafar and Scarif infecting a broad range of host species

Redefining development in Streptomyces venezuelae : integrating exploration into the classical sporulating life cycle

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