Phylogenetic Distribution of WhiB- and Lsr2-Type Regulators in Actinobacteriophage Genomes

Sharma, Vikas; Hardy, Aël; Luthe, Tom; Frunzke, Julia

doi:10.1128/spectrum.00727-21

Cited by 10 publications

(9 citation statements)

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“…Finally, we note that lsr2 homologues are present in many actinobacteriophage genomes including those of Mycobacterium , Gordonia , Streptomyces and Microbacterium 54 , 55 (Fig. 6a ), raising the possibility that phages encode these to counter host defence mechanisms involving loss of Lsr2 activity.…”

Section: Resultsmentioning

confidence: 99%

Mycobacterial nucleoid-associated protein Lsr2 is required for productive mycobacteriophage infection

et al. 2023

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Mycobacteriophages are a diverse group of viruses infecting Mycobacterium with substantial therapeutic potential. However, as this potential becomes realized, the molecular details of phage infection and mechanisms of resistance remain ill-defined. Here we use live-cell fluorescence microscopy to visualize the spatiotemporal dynamics of mycobacteriophage infection in single cells and populations, showing that infection is dependent on the host nucleoid-associated Lsr2 protein. Mycobacteriophages preferentially adsorb at Mycobacterium smegmatis sites of new cell wall synthesis and following DNA injection, Lsr2 reorganizes away from host replication foci to establish zones of phage DNA replication (ZOPR). Cells lacking Lsr2 proceed through to cell lysis when infected but fail to generate consecutive phage bursts that trigger epidemic spread of phage particles to neighbouring cells. Many mycobacteriophages code for their own Lsr2-related proteins, and although their roles are unknown, they do not rescue the loss of host Lsr2.

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Section: Resultsmentioning

confidence: 99%

Mycobacterial nucleoid-associated protein Lsr2 is required for productive mycobacteriophage infection

et al. 2023

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“…For Ankus, Byblos, and DekoNeimoidia infecting S. griseus , a gene coding for a DNA polymerase exonuclease subunit was found as well. Interestingly, Mandalore and Naboo harbour a gene coding for an FtsK-like protein, and Ankus, Byblos, DekoNeimoidia, and Naboo additionally encode WhiB-like and Lsr2-like transcriptional regulators, which are widespread in actinophages (Sharma et al, 2021). All genomes contain almost 80% of hypothetical proteins, emphasizing the large amount of ‘dark matter’ in actinobacteriophage genomes.…”

Section: Resultsmentioning

confidence: 99%

“…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).…”

Section: Discussionmentioning

confidence: 99%

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

Erdrich,

Luthe,

Kever

et al. 2024

Preprint

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Key features of the actinobacterial genusStreptomycesare multicellular, filamentous growth and production of a broad portfolio of bioactive molecules. These characteristics appear to play an important role in phage-host interactions and are modulated by phages during infection. To accelerate research of such interactions and the investigation of novel immune systems in multicellular bacteria, phage isolation, sequencing, and characterization are needed. This is a prerequisite for establishing systematic collections that appropriately cover phage diversity for comparative analyses. As part of a public outreach programme within the priority programme SPP 2330, involving local schools, we describe the isolation and characterization of five novelStreptomycessiphoviruses infectingS. griseus,S. venezuelae, andS. olivaceus. All isolates are virulent members of two existing genera and, additionally, establish a new genus in theStanwilliamsviridaefamily. In addition to an extensive set of tRNAs and proteins involved in phage replication, about 80% of phage genes encode hypothetical proteins, underlining the yet underexplored phage diversity and genomic dark matter still found in bacteriophages infecting actinobacteria. Taken together, phages Ankus, Byblos, DekoNeimoidia, Mandalore, and Naboo expand the phage diversity and contribute to ongoing research in the field ofStreptomycesphage-host interactions.

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“…5). A previous study of our group identified WhiB-(pfam02467) and Lsr2-type (pfam11774) regulators as most abundant transcriptional regulators encoded by actinobacteriophages genomes 51 . This is in line with the analysis of prophage genomes, where we found WhiB among the top twenty domains (Lsr2 at position 80, see Supplementary Tables S7, S8).…”

Section: Genomic Comparison Reveals a Remarkable Phylogenetic Diversi...mentioning

confidence: 92%

Systematic analysis of prophage elements in actinobacterial genomes reveals a remarkable phylogenetic diversity

Sharma

Hünnefeld

Luthe

et al. 2023

Sci Rep

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Actinobacteria represent one of the largest bacterial phyla harboring many species of high medical, biotechnological and ecological relevance. Prophage elements are major contributors to bacterial genome diversity and were shown to significantly shape bacterial fitness and host-microbe interactions. In this study, we performed a systematic analysis of prophage elements in 2406 complete actinobacterial genomes. Overall, 2106 prophage elements were predicted to be present in about 50% (1172/2406) of the analyzed datasets. Interestingly, these identified sequences compose a high prevalence of cryptic prophage elements, indicating genetic decay and domestication. Analysis of the sequence relationship of predicted prophages with known actinobacteriophage genomes revealed an exceptional high phylogenetic diversity of prophage elements. As a trend, we observed a higher prevalence of prophage elements in vicinity to the terminus. Analysis of the prophage-encoded gene functions revealed that prophage sequences significantly contribute to the bacterial antiviral immune system, but no biosynthetic gene clusters involved in the synthesis of known antiphage molecules were identified in prophage genomes. Overall, the current study highlights the remarkable diversity of prophages in actinobacterial genomes, with highly divergent prophages in actinobacterial genomes and thus provides an important basis for further investigation of phage-host interactions in this important bacterial phylum.

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Phylogenetic Distribution of WhiB- and Lsr2-Type Regulators in Actinobacteriophage Genomes

Abstract: Actinobacteriophages are viruses that infect bacterial species of the diverse phylum of Actinobacteria. Phages engage in a close relationship with their bacterial host.

Cited by 10 publications

References 50 publications

Mycobacterial nucleoid-associated protein Lsr2 is required for productive mycobacteriophage infection

Mycobacterial nucleoid-associated protein Lsr2 is required for productive mycobacteriophage infection

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

Systematic analysis of prophage elements in actinobacterial genomes reveals a remarkable phylogenetic diversity

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