Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals
The threat to public health posed by drug-resistant bacteria is rapidly increasing, as some of healthcare’s most potent antibiotics are becoming obsolete. Approximately two-thirds of the world’s antibiotics are derived from natural products produced by Streptomyces encoded biosynthetic gene clusters...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-01-01
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| Series: | PLoS ONE |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782336/?tool=EBI |
| _version_ | 1818715624145158144 |
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| author | Elizabeth T. Montaño Jason F. Nideffer Lauren Brumage Marcella Erb Julia Busch Lynley Fernandez Alan I. Derman John Paul Davis Elena Estrada Sharon Fu Danielle Le Aishwarya Vuppala Cassidy Tran Elaine Luterstein Shivani Lakkaraju Sriya Panchagnula Caroline Ren Jennifer Doan Sharon Tran Jamielyn Soriano Yuya Fujita Pranathi Gutala Quinn Fujii Minda Lee Anthony Bui Carleen Villarreal Samuel R. Shing Sean Kim Danielle Freeman Vipula Racha Alicia Ho Prianka Kumar Kian Falah Thomas Dawson Eray Enustun Amy Prichard Ana Gomez Kanika Khanna Shelly Trigg Kit Pogliano Joe Pogliano |
| author_facet | Elizabeth T. Montaño Jason F. Nideffer Lauren Brumage Marcella Erb Julia Busch Lynley Fernandez Alan I. Derman John Paul Davis Elena Estrada Sharon Fu Danielle Le Aishwarya Vuppala Cassidy Tran Elaine Luterstein Shivani Lakkaraju Sriya Panchagnula Caroline Ren Jennifer Doan Sharon Tran Jamielyn Soriano Yuya Fujita Pranathi Gutala Quinn Fujii Minda Lee Anthony Bui Carleen Villarreal Samuel R. Shing Sean Kim Danielle Freeman Vipula Racha Alicia Ho Prianka Kumar Kian Falah Thomas Dawson Eray Enustun Amy Prichard Ana Gomez Kanika Khanna Shelly Trigg Kit Pogliano Joe Pogliano |
| author_sort | Elizabeth T. Montaño |
| collection | DOAJ |
| description | The threat to public health posed by drug-resistant bacteria is rapidly increasing, as some of healthcare’s most potent antibiotics are becoming obsolete. Approximately two-thirds of the world’s antibiotics are derived from natural products produced by Streptomyces encoded biosynthetic gene clusters. Thus, to identify novel gene clusters, we sequenced the genomes of four bioactive Streptomyces strains isolated from the soil in San Diego County and used Bacterial Cytological Profiling adapted for agar plate culturing in order to examine the mechanisms of bacterial inhibition exhibited by these strains. In the four strains, we identified 104 biosynthetic gene clusters. Some of these clusters were predicted to produce previously studied antibiotics; however, the known mechanisms of these molecules could not fully account for the antibacterial activity exhibited by the strains, suggesting that novel clusters might encode antibiotics. When assessed for their ability to inhibit the growth of clinically isolated pathogens, three Streptomyces strains demonstrated activity against methicillin-resistant Staphylococcus aureus. Additionally, due to the utility of bacteriophages for genetically manipulating bacterial strains via transduction, we also isolated four new phages (BartholomewSD, IceWarrior, Shawty, and TrvxScott) against S. platensis. A genomic analysis of our phages revealed nearly 200 uncharacterized proteins, including a new site-specific serine integrase that could prove to be a useful genetic tool. Sequence analysis of the Streptomyces strains identified CRISPR-Cas systems and specific spacer sequences that allowed us to predict phage host ranges. Ultimately, this study identified Streptomyces strains with the potential to produce novel chemical matter as well as integrase-encoding phages that could potentially be used to manipulate these strains. |
| first_indexed | 2024-12-17T19:06:19Z |
| format | Article |
| id | doaj.art-bcd3e87b9a164bb89f842e8d8caa09f4 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-17T19:06:19Z |
| publishDate | 2022-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-bcd3e87b9a164bb89f842e8d8caa09f42022-12-21T21:35:59ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01171Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenalsElizabeth T. MontañoJason F. NidefferLauren BrumageMarcella ErbJulia BuschLynley FernandezAlan I. DermanJohn Paul DavisElena EstradaSharon FuDanielle LeAishwarya VuppalaCassidy TranElaine LutersteinShivani LakkarajuSriya PanchagnulaCaroline RenJennifer DoanSharon TranJamielyn SorianoYuya FujitaPranathi GutalaQuinn FujiiMinda LeeAnthony BuiCarleen VillarrealSamuel R. ShingSean KimDanielle FreemanVipula RachaAlicia HoPrianka KumarKian FalahThomas DawsonEray EnustunAmy PrichardAna GomezKanika KhannaShelly TriggKit PoglianoJoe PoglianoThe threat to public health posed by drug-resistant bacteria is rapidly increasing, as some of healthcare’s most potent antibiotics are becoming obsolete. Approximately two-thirds of the world’s antibiotics are derived from natural products produced by Streptomyces encoded biosynthetic gene clusters. Thus, to identify novel gene clusters, we sequenced the genomes of four bioactive Streptomyces strains isolated from the soil in San Diego County and used Bacterial Cytological Profiling adapted for agar plate culturing in order to examine the mechanisms of bacterial inhibition exhibited by these strains. In the four strains, we identified 104 biosynthetic gene clusters. Some of these clusters were predicted to produce previously studied antibiotics; however, the known mechanisms of these molecules could not fully account for the antibacterial activity exhibited by the strains, suggesting that novel clusters might encode antibiotics. When assessed for their ability to inhibit the growth of clinically isolated pathogens, three Streptomyces strains demonstrated activity against methicillin-resistant Staphylococcus aureus. Additionally, due to the utility of bacteriophages for genetically manipulating bacterial strains via transduction, we also isolated four new phages (BartholomewSD, IceWarrior, Shawty, and TrvxScott) against S. platensis. A genomic analysis of our phages revealed nearly 200 uncharacterized proteins, including a new site-specific serine integrase that could prove to be a useful genetic tool. Sequence analysis of the Streptomyces strains identified CRISPR-Cas systems and specific spacer sequences that allowed us to predict phage host ranges. Ultimately, this study identified Streptomyces strains with the potential to produce novel chemical matter as well as integrase-encoding phages that could potentially be used to manipulate these strains.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782336/?tool=EBI |
| spellingShingle | Elizabeth T. Montaño Jason F. Nideffer Lauren Brumage Marcella Erb Julia Busch Lynley Fernandez Alan I. Derman John Paul Davis Elena Estrada Sharon Fu Danielle Le Aishwarya Vuppala Cassidy Tran Elaine Luterstein Shivani Lakkaraju Sriya Panchagnula Caroline Ren Jennifer Doan Sharon Tran Jamielyn Soriano Yuya Fujita Pranathi Gutala Quinn Fujii Minda Lee Anthony Bui Carleen Villarreal Samuel R. Shing Sean Kim Danielle Freeman Vipula Racha Alicia Ho Prianka Kumar Kian Falah Thomas Dawson Eray Enustun Amy Prichard Ana Gomez Kanika Khanna Shelly Trigg Kit Pogliano Joe Pogliano Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals PLoS ONE |
| title | Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals |
| title_full | Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals |
| title_fullStr | Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals |
| title_full_unstemmed | Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals |
| title_short | Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals |
| title_sort | isolation and characterization of streptomyces bacteriophages and streptomyces strains encoding biosynthetic arsenals |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782336/?tool=EBI |
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