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Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages
BACKGROUND: Paenibacillus larvae is a Firmicute bacterium that causes American Foulbrood, a lethal disease in honeybees and is a major source of global agricultural losses. Although P. larvae phages were isolated prior to 2013, no full genome sequences of P. larvae bacteriophages were published or a...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4168068/ https://www.ncbi.nlm.nih.gov/pubmed/25174730 http://dx.doi.org/10.1186/1471-2164-15-745 |
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author | Merrill, Bryan D Grose, Julianne H Breakwell, Donald P Burnett, Sandra H |
author_facet | Merrill, Bryan D Grose, Julianne H Breakwell, Donald P Burnett, Sandra H |
author_sort | Merrill, Bryan D |
collection | PubMed |
description | BACKGROUND: Paenibacillus larvae is a Firmicute bacterium that causes American Foulbrood, a lethal disease in honeybees and is a major source of global agricultural losses. Although P. larvae phages were isolated prior to 2013, no full genome sequences of P. larvae bacteriophages were published or analyzed. This report includes an in-depth analysis of the structure, genomes, and relatedness of P. larvae myoviruses Abouo, Davis, Emery, Jimmer1, Jimmer2, and siphovirus phiIBB_Pl23 to each other and to other known phages. RESULTS: P. larvae phages Abouo, Davies, Emery, Jimmer1, and Jimmer2 are myoviruses with ~50 kbp genomes. The six P. larvae phages form three distinct groups by dotplot analysis. An annotated linear genome map of these six phages displays important identifiable genes and demonstrates the relationship between phages. Sixty phage assembly or structural protein genes and 133 regulatory or other non-structural protein genes were identifiable among the six P. larvae phages. Jimmer1, Jimmer2, and Davies formed stable lysogens resistant to superinfection by genetically similar phages. The correlation between tape measure protein gene length and phage tail length allowed identification of co-isolated phages Emery and Abouo in electron micrographs. A Phamerator database was assembled with the P. larvae phage genomes and 107 genomes of Firmicute-infecting phages, including 71 Bacillus phages. Phamerator identified conserved domains in 1,501 of 6,181 phamilies (only 24.3%) encoded by genes in the database and revealed that P. larvae phage genomes shared at least one phamily with 72 of the 107 other phages. The phamily relationship of large terminase proteins was used to indicate putative DNA packaging strategies. Analyses from CoreGenes, Phamerator, and electron micrograph measurements indicated Jimmer1, Jimmer2, Abouo and Davies were related to phages phiC2, EJ-1, KC5a, and AQ113, which are small-genome myoviruses that infect Streptococcus, Lactobacillus, and Clostridium, respectively. CONCLUSIONS: This paper represents the first comparison of phage genomes in the Paenibacillus genus and the first organization of P. larvae phages based on sequence and structure. This analysis provides an important contribution to the field of bacteriophage genomics by serving as a foundation on which to build an understanding of the natural predators of P. larvae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-745) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4168068 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-41680682014-09-20 Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages Merrill, Bryan D Grose, Julianne H Breakwell, Donald P Burnett, Sandra H BMC Genomics Research Article BACKGROUND: Paenibacillus larvae is a Firmicute bacterium that causes American Foulbrood, a lethal disease in honeybees and is a major source of global agricultural losses. Although P. larvae phages were isolated prior to 2013, no full genome sequences of P. larvae bacteriophages were published or analyzed. This report includes an in-depth analysis of the structure, genomes, and relatedness of P. larvae myoviruses Abouo, Davis, Emery, Jimmer1, Jimmer2, and siphovirus phiIBB_Pl23 to each other and to other known phages. RESULTS: P. larvae phages Abouo, Davies, Emery, Jimmer1, and Jimmer2 are myoviruses with ~50 kbp genomes. The six P. larvae phages form three distinct groups by dotplot analysis. An annotated linear genome map of these six phages displays important identifiable genes and demonstrates the relationship between phages. Sixty phage assembly or structural protein genes and 133 regulatory or other non-structural protein genes were identifiable among the six P. larvae phages. Jimmer1, Jimmer2, and Davies formed stable lysogens resistant to superinfection by genetically similar phages. The correlation between tape measure protein gene length and phage tail length allowed identification of co-isolated phages Emery and Abouo in electron micrographs. A Phamerator database was assembled with the P. larvae phage genomes and 107 genomes of Firmicute-infecting phages, including 71 Bacillus phages. Phamerator identified conserved domains in 1,501 of 6,181 phamilies (only 24.3%) encoded by genes in the database and revealed that P. larvae phage genomes shared at least one phamily with 72 of the 107 other phages. The phamily relationship of large terminase proteins was used to indicate putative DNA packaging strategies. Analyses from CoreGenes, Phamerator, and electron micrograph measurements indicated Jimmer1, Jimmer2, Abouo and Davies were related to phages phiC2, EJ-1, KC5a, and AQ113, which are small-genome myoviruses that infect Streptococcus, Lactobacillus, and Clostridium, respectively. CONCLUSIONS: This paper represents the first comparison of phage genomes in the Paenibacillus genus and the first organization of P. larvae phages based on sequence and structure. This analysis provides an important contribution to the field of bacteriophage genomics by serving as a foundation on which to build an understanding of the natural predators of P. larvae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-745) contains supplementary material, which is available to authorized users. BioMed Central 2014-08-30 /pmc/articles/PMC4168068/ /pubmed/25174730 http://dx.doi.org/10.1186/1471-2164-15-745 Text en © Merrill et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Merrill, Bryan D Grose, Julianne H Breakwell, Donald P Burnett, Sandra H Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
title | Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
title_full | Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
title_fullStr | Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
title_full_unstemmed | Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
title_short | Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
title_sort | characterization of paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4168068/ https://www.ncbi.nlm.nih.gov/pubmed/25174730 http://dx.doi.org/10.1186/1471-2164-15-745 |
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