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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...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782336/ https://www.ncbi.nlm.nih.gov/pubmed/35061755 http://dx.doi.org/10.1371/journal.pone.0262354 |
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author | Montaño, Elizabeth T. Nideffer, Jason F. Brumage, Lauren Erb, Marcella Busch, Julia Fernandez, Lynley Derman, Alan I. Davis, John Paul Estrada, Elena Fu, Sharon Le, Danielle Vuppala, Aishwarya Tran, Cassidy Luterstein, Elaine Lakkaraju, Shivani Panchagnula, Sriya Ren, Caroline Doan, Jennifer Tran, Sharon Soriano, Jamielyn Fujita, Yuya Gutala, Pranathi Fujii, Quinn Lee, Minda Bui, Anthony Villarreal, Carleen Shing, Samuel R. Kim, Sean Freeman, Danielle Racha, Vipula Ho, Alicia Kumar, Prianka Falah, Kian Dawson, Thomas Enustun, Eray Prichard, Amy Gomez, Ana Khanna, Kanika Trigg, Shelly Pogliano, Kit Pogliano, Joe |
author_facet | Montaño, Elizabeth T. Nideffer, Jason F. Brumage, Lauren Erb, Marcella Busch, Julia Fernandez, Lynley Derman, Alan I. Davis, John Paul Estrada, Elena Fu, Sharon Le, Danielle Vuppala, Aishwarya Tran, Cassidy Luterstein, Elaine Lakkaraju, Shivani Panchagnula, Sriya Ren, Caroline Doan, Jennifer Tran, Sharon Soriano, Jamielyn Fujita, Yuya Gutala, Pranathi Fujii, Quinn Lee, Minda Bui, Anthony Villarreal, Carleen Shing, Samuel R. Kim, Sean Freeman, Danielle Racha, Vipula Ho, Alicia Kumar, Prianka Falah, Kian Dawson, Thomas Enustun, Eray Prichard, Amy Gomez, Ana Khanna, Kanika Trigg, Shelly Pogliano, Kit Pogliano, Joe |
author_sort | Montaño, Elizabeth T. |
collection | PubMed |
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. |
format | Online Article Text |
id | pubmed-8782336 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-87823362022-01-22 Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals Montaño, Elizabeth T. Nideffer, Jason F. Brumage, Lauren Erb, Marcella Busch, Julia Fernandez, Lynley Derman, Alan I. Davis, John Paul Estrada, Elena Fu, Sharon Le, Danielle Vuppala, Aishwarya Tran, Cassidy Luterstein, Elaine Lakkaraju, Shivani Panchagnula, Sriya Ren, Caroline Doan, Jennifer Tran, Sharon Soriano, Jamielyn Fujita, Yuya Gutala, Pranathi Fujii, Quinn Lee, Minda Bui, Anthony Villarreal, Carleen Shing, Samuel R. Kim, Sean Freeman, Danielle Racha, Vipula Ho, Alicia Kumar, Prianka Falah, Kian Dawson, Thomas Enustun, Eray Prichard, Amy Gomez, Ana Khanna, Kanika Trigg, Shelly Pogliano, Kit Pogliano, Joe PLoS One Research Article 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. Public Library of Science 2022-01-21 /pmc/articles/PMC8782336/ /pubmed/35061755 http://dx.doi.org/10.1371/journal.pone.0262354 Text en © 2022 Montaño et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Montaño, Elizabeth T. Nideffer, Jason F. Brumage, Lauren Erb, Marcella Busch, Julia Fernandez, Lynley Derman, Alan I. Davis, John Paul Estrada, Elena Fu, Sharon Le, Danielle Vuppala, Aishwarya Tran, Cassidy Luterstein, Elaine Lakkaraju, Shivani Panchagnula, Sriya Ren, Caroline Doan, Jennifer Tran, Sharon Soriano, Jamielyn Fujita, Yuya Gutala, Pranathi Fujii, Quinn Lee, Minda Bui, Anthony Villarreal, Carleen Shing, Samuel R. Kim, Sean Freeman, Danielle Racha, Vipula Ho, Alicia Kumar, Prianka Falah, Kian Dawson, Thomas Enustun, Eray Prichard, Amy Gomez, Ana Khanna, Kanika Trigg, Shelly Pogliano, Kit Pogliano, Joe Isolation and characterization of Streptomyces bacteriophages and Streptomyces strains encoding biosynthetic arsenals |
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 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8782336/ https://www.ncbi.nlm.nih.gov/pubmed/35061755 http://dx.doi.org/10.1371/journal.pone.0262354 |
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