When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens

Dickeya solani and Pectobacterium carotovorum subsp. brasiliense are recently established species of bacterial plant pathogens causing black leg and soft rot of many vegetables and ornamental plants. Pseudomonas sp. strain P482 inhibits the growth of these pathogens, a desired trait considering the...

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Main Authors: Krzyżanowska, Dorota M., Ossowicki, Adam, Rajewska, Magdalena, Maciąg, Tomasz, Jabłońska, Magdalena, Obuchowski, Michał, Heeb, Stephan, Jafra, Sylwia
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Published: Frontiers 2016
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Online Access:https://eprints.nottingham.ac.uk/35186/
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author Krzyżanowska, Dorota M.
Ossowicki, Adam
Rajewska, Magdalena
Maciąg, Tomasz
Jabłońska, Magdalena
Obuchowski, Michał
Heeb, Stephan
Jafra, Sylwia
author_facet Krzyżanowska, Dorota M.
Ossowicki, Adam
Rajewska, Magdalena
Maciąg, Tomasz
Jabłońska, Magdalena
Obuchowski, Michał
Heeb, Stephan
Jafra, Sylwia
author_sort Krzyżanowska, Dorota M.
building Nottingham Research Data Repository
collection Online Access
description Dickeya solani and Pectobacterium carotovorum subsp. brasiliense are recently established species of bacterial plant pathogens causing black leg and soft rot of many vegetables and ornamental plants. Pseudomonas sp. strain P482 inhibits the growth of these pathogens, a desired trait considering the limited measures to combat these diseases. In this study, we determined the genetic background of the antibacterial activity of P482, and established the phylogenetic position of this strain. Pseudomonas sp. P482 was classified as Pseudomonas donghuensis. Genome mining revealed that the P482 genome does not contain genes determining the synthesis of known antimicrobials. However, the ClusterFinder algorithm, designed to detect atypical or novel classes of secondary metabolite gene clusters, predicted 18 such clusters in the genome. Screening of a Tn5 mutant library yielded an antimicrobial negative transposon mutant. The transposon insertion was located in a gene encoding an HpcH/HpaI aldolase/citrate lyase family protein. This gene is located in a hypothetical cluster predicted by the ClusterFinder, together with the downstream homologs of four nfs genes, that confer production of a non-fluorescent siderophore by P. donghuensis HYS(T). Site-directed inactivation of the HpcH/HpaI aldolase gene, the adjacent short chain dehydrogenase gene, as well as a homolog of an essential nfs cluster gene, all abolished the antimicrobial activity of the P482, suggesting their involvement in a common biosynthesis pathway. However, none of the mutants showed a decreased siderophore yield, neither was the antimicrobial activity of the wild type P482 compromised by high iron bioavailability. A genomic region comprising the nfs cluster and three upstream genes is involved in the antibacterial activity of P. donghuensis P482 against D. solani and P. carotovorum subsp. brasiliense. The genes studied are unique to the two known P. donghuensis strains. This study illustrates that mining of microbial genomes is a powerful approach for predictingthe presence of novel secondary-metabolite encoding genes especially when coupled with transposon mutagenesis.
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spelling nottingham-351862020-05-04T17:50:16Z https://eprints.nottingham.ac.uk/35186/ When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens Krzyżanowska, Dorota M. Ossowicki, Adam Rajewska, Magdalena Maciąg, Tomasz Jabłońska, Magdalena Obuchowski, Michał Heeb, Stephan Jafra, Sylwia Dickeya solani and Pectobacterium carotovorum subsp. brasiliense are recently established species of bacterial plant pathogens causing black leg and soft rot of many vegetables and ornamental plants. Pseudomonas sp. strain P482 inhibits the growth of these pathogens, a desired trait considering the limited measures to combat these diseases. In this study, we determined the genetic background of the antibacterial activity of P482, and established the phylogenetic position of this strain. Pseudomonas sp. P482 was classified as Pseudomonas donghuensis. Genome mining revealed that the P482 genome does not contain genes determining the synthesis of known antimicrobials. However, the ClusterFinder algorithm, designed to detect atypical or novel classes of secondary metabolite gene clusters, predicted 18 such clusters in the genome. Screening of a Tn5 mutant library yielded an antimicrobial negative transposon mutant. The transposon insertion was located in a gene encoding an HpcH/HpaI aldolase/citrate lyase family protein. This gene is located in a hypothetical cluster predicted by the ClusterFinder, together with the downstream homologs of four nfs genes, that confer production of a non-fluorescent siderophore by P. donghuensis HYS(T). Site-directed inactivation of the HpcH/HpaI aldolase gene, the adjacent short chain dehydrogenase gene, as well as a homolog of an essential nfs cluster gene, all abolished the antimicrobial activity of the P482, suggesting their involvement in a common biosynthesis pathway. However, none of the mutants showed a decreased siderophore yield, neither was the antimicrobial activity of the wild type P482 compromised by high iron bioavailability. A genomic region comprising the nfs cluster and three upstream genes is involved in the antibacterial activity of P. donghuensis P482 against D. solani and P. carotovorum subsp. brasiliense. The genes studied are unique to the two known P. donghuensis strains. This study illustrates that mining of microbial genomes is a powerful approach for predictingthe presence of novel secondary-metabolite encoding genes especially when coupled with transposon mutagenesis. Frontiers 2016-05-26 Article PeerReviewed Krzyżanowska, Dorota M., Ossowicki, Adam, Rajewska, Magdalena, Maciąg, Tomasz, Jabłońska, Magdalena, Obuchowski, Michał, Heeb, Stephan and Jafra, Sylwia (2016) When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens. Frontiers in Microbiology, 7 . 782/1-728/18. ISSN 1664-302X Dickeya Pectobacterium secondary metabolites genome mining antiSMASH nfs http://journal.frontiersin.org/article/10.3389/fmicb.2016.00782/full doi:10.3389/fmicb.2016.00782 doi:10.3389/fmicb.2016.00782
spellingShingle Dickeya
Pectobacterium
secondary metabolites
genome mining
antiSMASH
nfs
Krzyżanowska, Dorota M.
Ossowicki, Adam
Rajewska, Magdalena
Maciąg, Tomasz
Jabłońska, Magdalena
Obuchowski, Michał
Heeb, Stephan
Jafra, Sylwia
When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens
title When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens
title_full When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens
title_fullStr When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens
title_full_unstemmed When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens
title_short When genome-based approach meets the “Old but Good”: revealing genes involved in the antibacterial activity of Pseudomonas sp. P482 against soft rot pathogens
title_sort when genome-based approach meets the “old but good”: revealing genes involved in the antibacterial activity of pseudomonas sp. p482 against soft rot pathogens
topic Dickeya
Pectobacterium
secondary metabolites
genome mining
antiSMASH
nfs
url https://eprints.nottingham.ac.uk/35186/
https://eprints.nottingham.ac.uk/35186/
https://eprints.nottingham.ac.uk/35186/