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Exploratory growth in Streptomyces venezuelae involves a unique transcriptional program, enhanced oxidative stress response, and profound acceleration in response to glycerol

Evan M. F. Shepherdson, Tina Netzker, Yordan Stoyanov, View ORCID ProfileMarie A. Elliot
doi: https://doi.org/10.1101/2021.12.22.473798
Evan M. F. Shepherdson
1Department of Biochemistry & Biomedical Sciences, and M.G. DeGroote Institute for Infectious Disease Research, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1
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Tina Netzker
2Department of Biology, and M.G. DeGroote Institute for Infectious Disease Research, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1
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Yordan Stoyanov
2Department of Biology, and M.G. DeGroote Institute for Infectious Disease Research, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1
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Marie A. Elliot
2Department of Biology, and M.G. DeGroote Institute for Infectious Disease Research, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1
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  • ORCID record for Marie A. Elliot
  • For correspondence: melliot@mcmaster.ca
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ABSTRACT

Exploration is a recently discovered mode of growth and behaviour exhibited by some Streptomyces species that is distinct from their classical sporulating life cycle. While much has been uncovered regarding initiating environmental conditions and the phenotypic outcomes of exploratory growth, how this process is coordinated at a genetic level remains unclear. We used RNA-sequencing to survey global changes in the transcriptional profile of exploring cultures over time in the model organism Streptomyces venezuelae. Transcriptomic analyses revealed widespread changes in gene expression impacting diverse cellular functions. Investigations into differentially expressed regulatory elements revealed specific groups of regulatory factors to be impacted, including the expression of several extracytoplasmic function (ECF) sigma factors, second messenger signalling pathways, and members of the whiB-like (wbl) family of transcription factors. Dramatic changes were observed among primary metabolic pathways, especially among respiration-associated genes and the oxidative stress response; enzyme assays confirmed that exploring cultures exhibit an enhanced oxidative stress response compared with classically growing cultures. Changes in expression of the glycerol catabolic genes in S. venezuelae led to the discovery that glycerol supplementation of the growth medium promotes a dramatic acceleration of exploration. This effect appears to be unique to glycerol as an alternative carbon source and this response is broadly conserved across other exploration-competent species.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 22, 2021.
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Exploratory growth in Streptomyces venezuelae involves a unique transcriptional program, enhanced oxidative stress response, and profound acceleration in response to glycerol
Evan M. F. Shepherdson, Tina Netzker, Yordan Stoyanov, Marie A. Elliot
bioRxiv 2021.12.22.473798; doi: https://doi.org/10.1101/2021.12.22.473798
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Exploratory growth in Streptomyces venezuelae involves a unique transcriptional program, enhanced oxidative stress response, and profound acceleration in response to glycerol
Evan M. F. Shepherdson, Tina Netzker, Yordan Stoyanov, Marie A. Elliot
bioRxiv 2021.12.22.473798; doi: https://doi.org/10.1101/2021.12.22.473798

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