Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
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
_version_ 1784638291175276544
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
work_keys_str_mv AT montanoelizabetht isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT nidefferjasonf isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT brumagelauren isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT erbmarcella isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT buschjulia isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT fernandezlynley isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT dermanalani isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT davisjohnpaul isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT estradaelena isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT fusharon isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT ledanielle isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT vuppalaaishwarya isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT trancassidy isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT lutersteinelaine isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT lakkarajushivani isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT panchagnulasriya isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT rencaroline isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT doanjennifer isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT transharon isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT sorianojamielyn isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT fujitayuya isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT gutalapranathi isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT fujiiquinn isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT leeminda isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT buianthony isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT villarrealcarleen isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT shingsamuelr isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT kimsean isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT freemandanielle isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT rachavipula isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT hoalicia isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT kumarprianka isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT falahkian isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT dawsonthomas isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT enustuneray isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT prichardamy isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT gomezana isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT khannakanika isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT triggshelly isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT poglianokit isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals
AT poglianojoe isolationandcharacterizationofstreptomycesbacteriophagesandstreptomycesstrainsencodingbiosyntheticarsenals