Genome annotation and antimicrobial properties of Bacillus toyonensis VU-DES13, isolated from the Folsomia candida gut

Valeria Agamennone, Joeri van Straalen, Abraham Brouwer, Tjalf E. de Boer, Paul J. Hensbergen, Niels Zaagman, Martin Braster, Nico M. van Straalen, Dick Roelofs, Thierry K.S. Janssens

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Antibiotic resistance necessitates the search for new bioactive compounds with novel mechanisms of action. Natural products derived from bacteria and fungi are widely used in the field of medicine and new environments can be explored as sources of antimicrobials. Bacteria associated with springtails have shown high inhibitory activity against pathogens. Here, we characterized a bacterial strain with high potential for antimicrobial activity, isolated from the gut of the springtail Folsomia candida Willem (Collembola: Isotomidae). The strain was characterized using the ‘analytical profile index’ and the ‘minimal inhibitory concentration’ assay to test for antibiotic resistance. Agar overlay and agar disk diffusion assays were used to test the inhibitory activity of the strain and its extract against a variety of pathogens, and reporter assays were used to investigate the mode of action. High-performance liquid chromatography was used to analyze and fractionate the extract of bacterial culture, followed by additional assays on the fractions. The genome of the strain was screened for presence of antibiotic resistance genes and secondary metabolite gene clusters. The isolate was identified as Bacillus toyonensis Jiménez et al., but it displayed differences in metabolic profile when compared to the type species. The isolate was highly resistant to penicillin and inhibited the growth of a variety of pathogenic microorganisms. Genome analysis revealed an enrichment of resistance genes for β-lactam antibiotics compared to the type isolate. Also, secondary metabolite clusters involved in the production of siderophores, bacteriocins, and nonribosomal peptide synthetases were identified. In conclusion, a unique Bacillus strain was isolated from the gut of F. candida, for which we provide evidence of inhibitory activity against an array of pathogens. This, coupled with high resistance to penicillin as substantiated by the presence of resistance genes, points to the potential of B. toyonensis VU-DES13 to provide a new source of antimicrobial compounds.

Original languageEnglish
Pages (from-to)269-285
Number of pages17
JournalEntomologia experimentalis et applicata
Volume167
Issue number3
Early online date4 Mar 2019
DOIs
Publication statusPublished - Mar 2019

Fingerprint

Folsomia candida
anti-infective properties
antibiotic resistance
genome
digestive system
assay
Collembola
pathogen
gene
secondary metabolite
agar
anti-infective agents
assays
penicillins
secondary metabolites
pathogens
mechanism of action
siderophore
bacterium
antimicrobial activity

Bibliographical note

Special Issue: Symbionts in Insect Biology and Pest Control

Keywords

  • antibiotic resistance
  • Collembola
  • colonization resistance
  • inhibition
  • Isotomidae
  • pathogens
  • springtail

Cite this

Agamennone, Valeria ; van Straalen, Joeri ; Brouwer, Abraham ; de Boer, Tjalf E. ; Hensbergen, Paul J. ; Zaagman, Niels ; Braster, Martin ; van Straalen, Nico M. ; Roelofs, Dick ; Janssens, Thierry K.S. / Genome annotation and antimicrobial properties of Bacillus toyonensis VU-DES13, isolated from the Folsomia candida gut. In: Entomologia experimentalis et applicata. 2019 ; Vol. 167, No. 3. pp. 269-285.
@article{0deab267cf86457a90b86b7b8491d6a6,
title = "Genome annotation and antimicrobial properties of Bacillus toyonensis VU-DES13, isolated from the Folsomia candida gut",
abstract = "Antibiotic resistance necessitates the search for new bioactive compounds with novel mechanisms of action. Natural products derived from bacteria and fungi are widely used in the field of medicine and new environments can be explored as sources of antimicrobials. Bacteria associated with springtails have shown high inhibitory activity against pathogens. Here, we characterized a bacterial strain with high potential for antimicrobial activity, isolated from the gut of the springtail Folsomia candida Willem (Collembola: Isotomidae). The strain was characterized using the ‘analytical profile index’ and the ‘minimal inhibitory concentration’ assay to test for antibiotic resistance. Agar overlay and agar disk diffusion assays were used to test the inhibitory activity of the strain and its extract against a variety of pathogens, and reporter assays were used to investigate the mode of action. High-performance liquid chromatography was used to analyze and fractionate the extract of bacterial culture, followed by additional assays on the fractions. The genome of the strain was screened for presence of antibiotic resistance genes and secondary metabolite gene clusters. The isolate was identified as Bacillus toyonensis Jim{\'e}nez et al., but it displayed differences in metabolic profile when compared to the type species. The isolate was highly resistant to penicillin and inhibited the growth of a variety of pathogenic microorganisms. Genome analysis revealed an enrichment of resistance genes for β-lactam antibiotics compared to the type isolate. Also, secondary metabolite clusters involved in the production of siderophores, bacteriocins, and nonribosomal peptide synthetases were identified. In conclusion, a unique Bacillus strain was isolated from the gut of F. candida, for which we provide evidence of inhibitory activity against an array of pathogens. This, coupled with high resistance to penicillin as substantiated by the presence of resistance genes, points to the potential of B. toyonensis VU-DES13 to provide a new source of antimicrobial compounds.",
keywords = "antibiotic resistance, Collembola, colonization resistance, inhibition, Isotomidae, pathogens, springtail",
author = "Valeria Agamennone and {van Straalen}, Joeri and Abraham Brouwer and {de Boer}, {Tjalf E.} and Hensbergen, {Paul J.} and Niels Zaagman and Martin Braster and {van Straalen}, {Nico M.} and Dick Roelofs and Janssens, {Thierry K.S.}",
note = "Special Issue: Symbionts in Insect Biology and Pest Control",
year = "2019",
month = "3",
doi = "10.1111/eea.12763",
language = "English",
volume = "167",
pages = "269--285",
journal = "Entomologia experimentalis et applicata",
issn = "0013-8703",
publisher = "Wiley-Blackwell",
number = "3",

}

Genome annotation and antimicrobial properties of Bacillus toyonensis VU-DES13, isolated from the Folsomia candida gut. / Agamennone, Valeria; van Straalen, Joeri; Brouwer, Abraham; de Boer, Tjalf E.; Hensbergen, Paul J.; Zaagman, Niels; Braster, Martin; van Straalen, Nico M.; Roelofs, Dick; Janssens, Thierry K.S.

In: Entomologia experimentalis et applicata, Vol. 167, No. 3, 03.2019, p. 269-285.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Genome annotation and antimicrobial properties of Bacillus toyonensis VU-DES13, isolated from the Folsomia candida gut

AU - Agamennone, Valeria

AU - van Straalen, Joeri

AU - Brouwer, Abraham

AU - de Boer, Tjalf E.

AU - Hensbergen, Paul J.

AU - Zaagman, Niels

AU - Braster, Martin

AU - van Straalen, Nico M.

AU - Roelofs, Dick

AU - Janssens, Thierry K.S.

N1 - Special Issue: Symbionts in Insect Biology and Pest Control

PY - 2019/3

Y1 - 2019/3

N2 - Antibiotic resistance necessitates the search for new bioactive compounds with novel mechanisms of action. Natural products derived from bacteria and fungi are widely used in the field of medicine and new environments can be explored as sources of antimicrobials. Bacteria associated with springtails have shown high inhibitory activity against pathogens. Here, we characterized a bacterial strain with high potential for antimicrobial activity, isolated from the gut of the springtail Folsomia candida Willem (Collembola: Isotomidae). The strain was characterized using the ‘analytical profile index’ and the ‘minimal inhibitory concentration’ assay to test for antibiotic resistance. Agar overlay and agar disk diffusion assays were used to test the inhibitory activity of the strain and its extract against a variety of pathogens, and reporter assays were used to investigate the mode of action. High-performance liquid chromatography was used to analyze and fractionate the extract of bacterial culture, followed by additional assays on the fractions. The genome of the strain was screened for presence of antibiotic resistance genes and secondary metabolite gene clusters. The isolate was identified as Bacillus toyonensis Jiménez et al., but it displayed differences in metabolic profile when compared to the type species. The isolate was highly resistant to penicillin and inhibited the growth of a variety of pathogenic microorganisms. Genome analysis revealed an enrichment of resistance genes for β-lactam antibiotics compared to the type isolate. Also, secondary metabolite clusters involved in the production of siderophores, bacteriocins, and nonribosomal peptide synthetases were identified. In conclusion, a unique Bacillus strain was isolated from the gut of F. candida, for which we provide evidence of inhibitory activity against an array of pathogens. This, coupled with high resistance to penicillin as substantiated by the presence of resistance genes, points to the potential of B. toyonensis VU-DES13 to provide a new source of antimicrobial compounds.

AB - Antibiotic resistance necessitates the search for new bioactive compounds with novel mechanisms of action. Natural products derived from bacteria and fungi are widely used in the field of medicine and new environments can be explored as sources of antimicrobials. Bacteria associated with springtails have shown high inhibitory activity against pathogens. Here, we characterized a bacterial strain with high potential for antimicrobial activity, isolated from the gut of the springtail Folsomia candida Willem (Collembola: Isotomidae). The strain was characterized using the ‘analytical profile index’ and the ‘minimal inhibitory concentration’ assay to test for antibiotic resistance. Agar overlay and agar disk diffusion assays were used to test the inhibitory activity of the strain and its extract against a variety of pathogens, and reporter assays were used to investigate the mode of action. High-performance liquid chromatography was used to analyze and fractionate the extract of bacterial culture, followed by additional assays on the fractions. The genome of the strain was screened for presence of antibiotic resistance genes and secondary metabolite gene clusters. The isolate was identified as Bacillus toyonensis Jiménez et al., but it displayed differences in metabolic profile when compared to the type species. The isolate was highly resistant to penicillin and inhibited the growth of a variety of pathogenic microorganisms. Genome analysis revealed an enrichment of resistance genes for β-lactam antibiotics compared to the type isolate. Also, secondary metabolite clusters involved in the production of siderophores, bacteriocins, and nonribosomal peptide synthetases were identified. In conclusion, a unique Bacillus strain was isolated from the gut of F. candida, for which we provide evidence of inhibitory activity against an array of pathogens. This, coupled with high resistance to penicillin as substantiated by the presence of resistance genes, points to the potential of B. toyonensis VU-DES13 to provide a new source of antimicrobial compounds.

KW - antibiotic resistance

KW - Collembola

KW - colonization resistance

KW - inhibition

KW - Isotomidae

KW - pathogens

KW - springtail

UR - http://www.scopus.com/inward/record.url?scp=85062595907&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85062595907&partnerID=8YFLogxK

U2 - 10.1111/eea.12763

DO - 10.1111/eea.12763

M3 - Article

VL - 167

SP - 269

EP - 285

JO - Entomologia experimentalis et applicata

JF - Entomologia experimentalis et applicata

SN - 0013-8703

IS - 3

ER -