Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)

BackgroundThis paper brings new information about the genome and phenotypic characteristics of Pantoea agglomerans strain DBM 3797, isolated from fresh Czech hop (Humulus lupulus) in the Saaz hop-growing region. Although P. agglomerans strains are frequently isolated from different materials, there...

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Main Authors: Petra Patakova, Maryna Vasylkivska, Karel Sedlar, Katerina Jureckova, Matej Bezdicek, Petra Lovecka, Barbora Branska, Petr Kastanek, Karel Krofta
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1305338/full
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author Petra Patakova
Maryna Vasylkivska
Karel Sedlar
Karel Sedlar
Katerina Jureckova
Matej Bezdicek
Matej Bezdicek
Petra Lovecka
Barbora Branska
Petr Kastanek
Karel Krofta
author_facet Petra Patakova
Maryna Vasylkivska
Karel Sedlar
Karel Sedlar
Katerina Jureckova
Matej Bezdicek
Matej Bezdicek
Petra Lovecka
Barbora Branska
Petr Kastanek
Karel Krofta
author_sort Petra Patakova
collection DOAJ
description BackgroundThis paper brings new information about the genome and phenotypic characteristics of Pantoea agglomerans strain DBM 3797, isolated from fresh Czech hop (Humulus lupulus) in the Saaz hop-growing region. Although P. agglomerans strains are frequently isolated from different materials, there are not usually thoroughly characterized even if they have versatile metabolism and those isolated from plants may have a considerable potential for application in agriculture as a support culture for plant growth.MethodsP. agglomerans DBM 3797 was cultured under aerobic and anaerobic conditions, its metabolites were analyzed by HPLC and it was tested for plant growth promotion abilities, such as phosphate solubilization, siderophore and indol-3-acetic acid productions. In addition, genomic DNA was extracted, sequenced and de novo assembly was performed. Further, genome annotation, pan-genome analysis and selected genome analyses, such as CRISPR arrays detection, antibiotic resistance and secondary metabolite genes identification were carried out.Results and discussionThe typical appearance characteristics of the strain include the formation of symplasmata in submerged liquid culture and the formation of pale yellow colonies on agar. The genetic information of the strain (in total 4.8 Mb) is divided between a chromosome and two plasmids. The strain lacks any CRISPR-Cas system but is equipped with four restriction-modification systems. The phenotypic analysis focused on growth under both aerobic and anaerobic conditions, as well as traits associated with plant growth promotion. At both levels (genomic and phenotypic), the production of siderophores, indoleacetic acid-derived growth promoters, gluconic acid, and enzyme activities related to the degradation of complex organic compounds were found. Extracellular gluconic acid production under aerobic conditions (up to 8 g/l) is probably the result of glucose oxidation by the membrane-bound pyrroloquinoline quinone-dependent enzyme glucose dehydrogenase. The strain has a number of properties potentially beneficial to the hop plant and its closest relatives include the strains also isolated from the aerial parts of plants, yet its safety profile needs to be addressed in follow-up research.
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spelling doaj.art-14de8d50ef6549a7a0f97e3a143351442024-02-08T10:20:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-02-011510.3389/fmicb.2024.13053381305338Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)Petra Patakova0Maryna Vasylkivska1Karel Sedlar2Karel Sedlar3Katerina Jureckova4Matej Bezdicek5Matej Bezdicek6Petra Lovecka7Barbora Branska8Petr Kastanek9Karel Krofta10Department of Biotechnology, University of Chemistry and Technology Prague, Prague, CzechiaDepartment of Biotechnology, University of Chemistry and Technology Prague, Prague, CzechiaDepartment of Biomedical Engineering, Faculty of Electrical Engineering and Communication, Brno University of Technology, Brno, CzechiaDepartment of Informatics, Ludwig-Maximilians-Universität München, Munich, GermanyDepartment of Biomedical Engineering, Faculty of Electrical Engineering and Communication, Brno University of Technology, Brno, CzechiaDepartment of Internal Medicine—Hematology and Oncology, University Hospital Brno, Brno, CzechiaDepartment of Internal Medicine–Hematology and Oncology, Faculty of Medicine, Masaryk University, Brno, CzechiaDepartment of Biochemistry and Microbiology, University of Chemistry and Technology Prague, Prague, CzechiaDepartment of Biotechnology, University of Chemistry and Technology Prague, Prague, CzechiaEcofuel Laboratories s.r.o., Prague, CzechiaHop Research Institute, Co. Ltd., Zatec, CzechiaBackgroundThis paper brings new information about the genome and phenotypic characteristics of Pantoea agglomerans strain DBM 3797, isolated from fresh Czech hop (Humulus lupulus) in the Saaz hop-growing region. Although P. agglomerans strains are frequently isolated from different materials, there are not usually thoroughly characterized even if they have versatile metabolism and those isolated from plants may have a considerable potential for application in agriculture as a support culture for plant growth.MethodsP. agglomerans DBM 3797 was cultured under aerobic and anaerobic conditions, its metabolites were analyzed by HPLC and it was tested for plant growth promotion abilities, such as phosphate solubilization, siderophore and indol-3-acetic acid productions. In addition, genomic DNA was extracted, sequenced and de novo assembly was performed. Further, genome annotation, pan-genome analysis and selected genome analyses, such as CRISPR arrays detection, antibiotic resistance and secondary metabolite genes identification were carried out.Results and discussionThe typical appearance characteristics of the strain include the formation of symplasmata in submerged liquid culture and the formation of pale yellow colonies on agar. The genetic information of the strain (in total 4.8 Mb) is divided between a chromosome and two plasmids. The strain lacks any CRISPR-Cas system but is equipped with four restriction-modification systems. The phenotypic analysis focused on growth under both aerobic and anaerobic conditions, as well as traits associated with plant growth promotion. At both levels (genomic and phenotypic), the production of siderophores, indoleacetic acid-derived growth promoters, gluconic acid, and enzyme activities related to the degradation of complex organic compounds were found. Extracellular gluconic acid production under aerobic conditions (up to 8 g/l) is probably the result of glucose oxidation by the membrane-bound pyrroloquinoline quinone-dependent enzyme glucose dehydrogenase. The strain has a number of properties potentially beneficial to the hop plant and its closest relatives include the strains also isolated from the aerial parts of plants, yet its safety profile needs to be addressed in follow-up research.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1305338/fullPantoea agglomeranshops endophyteplant growth promotiongenome characterizationgluconic acid
spellingShingle Petra Patakova
Maryna Vasylkivska
Karel Sedlar
Karel Sedlar
Katerina Jureckova
Matej Bezdicek
Matej Bezdicek
Petra Lovecka
Barbora Branska
Petr Kastanek
Karel Krofta
Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)
Frontiers in Microbiology
Pantoea agglomerans
hops endophyte
plant growth promotion
genome characterization
gluconic acid
title Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)
title_full Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)
title_fullStr Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)
title_full_unstemmed Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)
title_short Whole genome sequencing and characterization of Pantoea agglomerans DBM 3797, endophyte, isolated from fresh hop (Humulus lupulus L.)
title_sort whole genome sequencing and characterization of pantoea agglomerans dbm 3797 endophyte isolated from fresh hop humulus lupulus l
topic Pantoea agglomerans
hops endophyte
plant growth promotion
genome characterization
gluconic acid
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1305338/full
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