Comparative Genomics of Three Novel Jumbo Bacteriophages Infecting Staphylococcus aureus

Korn, Abby; Hillhouse, Andrew; Sun, Lichang; Gill, Jason J.

doi:10.1128/jvi.02391-20

Cited by 15 publications

(13 citation statements)

References 78 publications

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“…However, many of the highly prevalent metatranscriptome-assembled vOTUs eluded recovery from the total metagenome. Recently it has become apparent that the hyper-modification of phage DNA prevents the sequencing of certain phage genomes [107, 108]. Subsequently, many phage genomes remain absent in DNA metagenomic samples prepared using transposon-based library methods, as used in this study.…”

Section: Discussionmentioning

confidence: 99%

Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

Muscatt

Hilton

Raguideau

et al. 2022

Preprint

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BackgroundThe rhizosphere is a hotspot for microbial activity and contributes to ecosystem services including plant health and biogeochemical cycling. The activity of microbial viruses, and their influence on plant-microbe interactions in the rhizosphere, remains undetermined. Given the impact of viruses on the ecology and evolution of their host communities, determining how soil viruses influence microbiome dynamics is crucial to build a holistic understanding of rhizosphere functions.ResultsHere, we aimed to investigate the influence of crop management on the composition and activity of bulk soil, rhizosphere soil, and root viral communities. We combined viromics, metagenomics, and metatranscriptomics on soil samples collected from a 3-year crop rotation field trial of oilseed rape (Brassica napus L.). By recovering 1,059 dsDNA viral populations and 16,541 ssRNA bacteriophage populations, we expanded the number of underexplored Leviviricetes genomes by > 5 times. Through detection of viral activity in metatranscriptomes, we uncovered evidence of “Kill-the-Winner” dynamics, implicating soil bacteriophages in driving bacterial community succession. Moreover, we found the activity of viruses increased with proximity to crop roots and identified that soil viruses may influence plant-microbe interactions through the reprogramming of bacterial host metabolism. We have provided the first evidence of crop rotation-driven impacts on soil microbial communities extending to viruses. To this aim, we present the novel principal of “viral priming”, which describes how the consecutive growth of the same crop species primes viral activity in the rhizosphere through local adaptation.ConclusionsOverall, we reveal unprecedented spatial and temporal diversity in viral community composition and activity across root, rhizosphere soil and bulk soil compartments. Our work demonstrates that the roles of soil viruses need greater consideration to exploit the rhizosphere microbiome for food security, food safety, and environmental sustainability.

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Section: Discussionmentioning

confidence: 99%

Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

Muscatt

Hilton

Raguideau

et al. 2022

Preprint

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“…Having one or more RNAP subunits may be an important feature of jumbo phages. Similarly, S. aureus jumbo phage MarsHill, classified as phiKZ-related phages, has 10 RNAP subunits, including 4 β subunits and 6 β′ subunits ( Korn et al, 2021 ). Staphylococcus phage PALS2 encoded 4 RNAP subunits, including β, β′, ω, and δ subunits ( Lee et al, 2021 ).…”

Section: Resultsmentioning

confidence: 99%

“…Therefore, 1 of 14 ORFs was supposed to encode holin-like protein, including ORF10, ORF24, ORF30, ORF38, ORF48, ORF84, ORF93-95, ORF117-119, ORF229, and ORF230. CDD results show that ORF117-encoded protein contained a holin_1 superfamily domain (cl02344) with an E value of 1.91e-08, so it was supposed to be holin because holin of Staphylococcus phage Machias has the highest identity of 64.94% with the protein encoded by ORF117 among these 14 ORFs ( Korn et al, 2021 ).…”

Section: Resultsmentioning

confidence: 99%

“…Staphylococcus jumbo phage PALS2 encoding 2 lysins (PALS2_239 and PALS2_240) can lyse various Staphylococcal strains, including S. aureus, S. haemolyticus , S. hominis , S. warneri , S. saprophyticus , S. capitis , and S. cohnii ( Lee et al, 2021 ). Three Staphylococcus jumbo phages, including Madawaska (ORF152 and ORF202), Machias (ORF154 and ORF213), and MarsHill (ORF152 and ORF203), share similar genomic characteristics and are also annotated as two lysins, but their lytic spectrum and bactericidal activities of lysins remain unclear ( Korn et al, 2021 ).…”

Section: Resultsmentioning

confidence: 99%

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Characterization and Genomic Analysis of a Novel Jumbo Bacteriophage vB_StaM_SA1 Infecting Staphylococcus aureus With Two Lysins

Zhang

Sun²,

Zhao

et al. 2022

Front. Microbiol.

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The development of new antimicrobial agents is critically needed due to the alarming increase in antibiotic resistance in bacterial pathogens. Phages have been widely considered as effective alternatives to antibiotics. A novel phage vB_StaM_SA1 (hereinafter as SA1) that can infect multiple Staphylococcus strains was isolated from untreated sewage of a pig farm, which belonged to Myoviridae family. At MOI of 0.1, the latent period of phage SA1 was 55 min, and the final titer reached about 109 PFU/mL. The genome of phage SA1 was 260,727 bp, indicating that it can be classified as a jumbo phage. The genome of SA1 had 258 ORFs and a serine tRNA, while only 53 ORFs were annotated with functions. Phage SA1 contained a group of core genes that was characterized by multiple RNA polymerase subunits and also found in phiKZ-related jumbo phages. The phylogenetic tree showed that phage SA1 was a phiKZ-related phage and was closer to jumbo phages compared with Staphylococcus phages with small genome. Three proteins (lys4, lys210, and lys211) were predicted to be associated with lysins, and two proteins with lytic function were verified by recombinant expression and bacterial survival test. Both lys210 and lys211 possessed efficient bactericidal ability, and lys210 could lyse all test strains. The results show that phage SA1 and lys210/lys211 could be potentially used as antibiotic agents to treat Staphylococcus infection.

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“…However, many of the highly prevalent metatranscriptome-assembled vOTUs eluded recovery from the total metagenome. Recently, it has become apparent that the hyper-modification of phage DNA prevents the sequencing of certain phage genomes [ 109 , 110 ]. Subsequently, many phage genomes remain absent in DNA metagenomic samples prepared using transposon-based library methods, as used in this study.…”

Section: Discussionmentioning

confidence: 99%

Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

et al. 2022

View full text Add to dashboard Cite

Background The rhizosphere is a hotspot for microbial activity and contributes to ecosystem services including plant health and biogeochemical cycling. The activity of microbial viruses, and their influence on plant-microbe interactions in the rhizosphere, remains undetermined. Given the impact of viruses on the ecology and evolution of their host communities, determining how soil viruses influence microbiome dynamics is crucial to build a holistic understanding of rhizosphere functions. Results Here, we aimed to investigate the influence of crop management on the composition and activity of bulk soil, rhizosphere soil, and root viral communities. We combined viromics, metagenomics, and metatranscriptomics on soil samples collected from a 3-year crop rotation field trial of oilseed rape (Brassica napus L.). By recovering 1059 dsDNA viral populations and 16,541 ssRNA bacteriophage populations, we expanded the number of underexplored Leviviricetes genomes by > 5 times. Through detection of viral activity in metatranscriptomes, we uncovered evidence of “Kill-the-Winner” dynamics, implicating soil bacteriophages in driving bacterial community succession. Moreover, we found the activity of viruses increased with proximity to crop roots, and identified that soil viruses may influence plant-microbe interactions through the reprogramming of bacterial host metabolism. We have provided the first evidence of crop rotation-driven impacts on soil microbial communities extending to viruses. To this aim, we present the novel principal of “viral priming,” which describes how the consecutive growth of the same crop species primes viral activity in the rhizosphere through local adaptation. Conclusions Overall, we reveal unprecedented spatial and temporal diversity in viral community composition and activity across root, rhizosphere soil, and bulk soil compartments. Our work demonstrates that the roles of soil viruses need greater consideration to exploit the rhizosphere microbiome for food security, food safety, and environmental sustainability.

show abstract

Comparative Genomics of Three Novel Jumbo Bacteriophages Infecting Staphylococcus aureus

Cited by 15 publications

References 78 publications

Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

Characterization and Genomic Analysis of a Novel Jumbo Bacteriophage vB_StaM_SA1 Infecting Staphylococcus aureus With Two Lysins

Crop management shapes the diversity and activity of DNA and RNA viruses in the rhizosphere

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