Genome sequence and characterization of five bacteriophages infectingStreptomyces coelicolorandStreptomyces venezuelae: Alderaan, Coruscant, Dagobah, Endor1 and Endor2

Abstract

Streptomyces are well-known antibiotic producers, and are also characterized by a complex morphological differentiation. Streptomyces, like all bacteria, are confronted with the constant threat of phage predation, which in turn shapes bacterial evolution. However, despite significant sequencing efforts recently, relatively few phages infecting Streptomyces have been characterized compared to other genera. Here, we present the isolation and characterization of five novel Streptomyces phages. All five phages belong to the Siphoviridae family, based on their morphology as determined by transmission electron microscopy. Genome sequencing revealed that four of them were temperate phages, while one had a lytic lifestyle. Moreover, one of the newly sequenced phages shows very little homology to already described phages, highlighting the still largely untapped viral diversity. Altogether, this study expands the number of characterized phages of Streptomyces and sheds light on phage evolution and phage-host dynamics in Streptomyces.

Expanding the phage galaxy: Isolation and characterization of five novel Streptomyces siphoviruses Ankus, Byblos, DekoNeimoidia, Mandalore, and Naboo

“…Focusing on the interaction between phages and specialized metabolite production, we observed red colouration of the S. albidoflavus (formerly S. coelicolor) lawn surrounding undiluted spots for Ankus, DekoNeimoidia, and Naboo. Enhanced actinorhodin production in response to phage infection was also observed in previous studies (Hardy et al, 2020; Kronheim et al, 2023). However, a direct antiphage function of actinorhodin has not been reported so far.…”

“…All of them exhibit an overall narrow host range based on the present analysis. Despite systematic phage host range analyses are not commonly standardized or done at all, it appears that S. venezuelae phages typically are very specific for their host as other phages like Alderaan and Coruscant (Hardy et al, 2020), which also show the same specificity infecting only one species like our newly isolated phage Mandalore. Interestingly, the observed host range of Ankus, Byblos, DekoNeimoidia and Naboo, all infecting both S. griseus and S. olivaceus , could be a more general feature.…”

“…Furthermore, Ankus, Byblos, DekoNeimoidia, Mandalore, and Naboo encode FtsK-like, Lsr2-like, and WhiB-like proteins known from host regulatory networks in Streptomyces , and which are found in many other actinobacteriophages (Bush, 2018; Chen and Banfield, 2024; Hardy et al, 2020; Sharma et al, 2021). Some other genomic features include a MazG-like pyrophosphatase in phage Mandalore, potentially interfering with the host abortive infection mechanism (Gross et al, 2006; Harms et al, 2018) and a Cas4 family exonuclease encoded by Naboo that could lead to host spacer acquisition and subsequently autoimmunity of the bacterial host (Hooton and Connerton, 2015).…”

“…The novel phage isolates were classified based on nucleotide sequence comparison against known Streptomyces phages (Hardy et al, 2020). Closely related bacteriophages were recovered from the NCBI nucleotide blast searches.…”

“…Surprisingly, phages, as the most abundant bacterial predator, have not yet been considered as a potential trigger of secondary metabolism. However, recent studies show the antiphage properties of Streptomyces -derived aminoglycosides and anthracyclines (Jiang et al, 2020; Kever et al, 2022; Kronheim et al, 2018), as well as initial phenomenological and transcriptional clues indicating that phage infection actually triggers the production of specialized metabolites (Hardy et al, 2020; Kronheim et al, 2023; Luthe et al, 2023).…”