Increased Biological Activity of Aneurinibacillus migulanus Strains Correlates with the Production of New Gramicidin Secondary Metabolites

Faizah N. Alenezi, Imen Rekik, Ali Chenari Bouket, Lenka Luptakova, Mostafa E. Rateb, Hedda J. Weitz, Marcel Jaspars, Stephen Woodward, Lassaad Belbahri

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Abstract

The soil-borne gram-positive bacteria Aneurinibacillus migulanus strain Nagano shows considerable potential as a biocontrol agent against plant diseases. In contrast, A. migulanus NCTC 7096 proved less effective for inhibition of plant pathogens. Nagano strain exerts biocontrol activity against some gram-positive and gram-negative bacteria, fungi and oomycetes through the production of gramicidin S (GS). Apart from the antibiotic effects, GS increases the rate of evaporation from the plant surface, reducing periods of surface wetness and thereby indirectly inhibiting spore germination. To elucidate the molecular basis of differential biocontrol abilities of Nagano and NCTC 7096, we compared GS production and biosurfactant secretion in addition to genome mining of the genomes. Our results proved that: (i) Using oil spreading, blood agar lysis, surface tension and tomato leaves wetness assays, Nagano showed increased biosurfactant secretion in comparison with NCTC 7096, (ii) Genome mining indicated the presence of GS genes in both Nagano and NCTC 7096 with two amino acid units difference between the strains: T342I and P419S. Using 3D models and the DUET server, T342I and P419S were predicted to decrease the stability of the NCTC 7096 GS synthase, (iii) Nagano produced two additional GS-like molecules GS-1155 (molecular weight 1155) and GS-1169 (molecular weight 1169), where one or two ornithine residues replace lysine in the peptide. There was also a negative correlation between surface tension and the quantity of GS-1169 present in Nagano, and (iv) the Nagano genome had a full protein network of exopolysaccharide biosynthesis in contrast to NCTC 7096 which lacked the first enzyme of the network. NCTC 7096 is unable to form biofilms as observed for Nagano. Different molecular layers, mainly gramicidin secondary metabolite production, account for differential biocontrol abilities of Nagano and NCTC 7096. This work highlighted the basis of differential biological control abilities between strains belonging to the same species and demonstrates techniques useful to the screening of effective biocontrol strains for environmentally friendly secondary metabolites that can be used to manage plant pathogens in the field.
Original languageEnglish
Article number517
Pages (from-to)1-11
Number of pages11
JournalFrontiers in Microbiology
Volume8
DOIs
Publication statusPublished - 7 Apr 2017

Fingerprint

Gramicidin
Genome
Surface Tension
Molecular Weight
Oomycetes
Plant Diseases
Ornithine
Gram-Positive Bacteria
Lycopersicon esculentum
Biofilms
Germination
Spores
Gram-Negative Bacteria
Lysine
Agar
Oils
Fungi
Soil
Anti-Bacterial Agents

Keywords

  • secondary metabolism
  • bioinformatics
  • genome mining
  • Aneurinibacillus migulanus
  • Biocontrol bacteria
  • Gramicidin S
  • biosurfactant

Cite this

Increased Biological Activity of Aneurinibacillus migulanus Strains Correlates with the Production of New Gramicidin Secondary Metabolites. / Alenezi, Faizah N.; Rekik, Imen; Bouket, Ali Chenari ; Luptakova, Lenka; Rateb, Mostafa E.; Weitz, Hedda J.; Jaspars, Marcel; Woodward, Stephen; Belbahri, Lassaad.

In: Frontiers in Microbiology, Vol. 8, 517, 07.04.2017, p. 1-11.

Research output: Contribution to journalArticle

Alenezi, Faizah N. ; Rekik, Imen ; Bouket, Ali Chenari ; Luptakova, Lenka ; Rateb, Mostafa E. ; Weitz, Hedda J. ; Jaspars, Marcel ; Woodward, Stephen ; Belbahri, Lassaad. / Increased Biological Activity of Aneurinibacillus migulanus Strains Correlates with the Production of New Gramicidin Secondary Metabolites. In: Frontiers in Microbiology. 2017 ; Vol. 8. pp. 1-11.
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abstract = "The soil-borne gram-positive bacteria Aneurinibacillus migulanus strain Nagano shows considerable potential as a biocontrol agent against plant diseases. In contrast, A. migulanus NCTC 7096 proved less effective for inhibition of plant pathogens. Nagano strain exerts biocontrol activity against some gram-positive and gram-negative bacteria, fungi and oomycetes through the production of gramicidin S (GS). Apart from the antibiotic effects, GS increases the rate of evaporation from the plant surface, reducing periods of surface wetness and thereby indirectly inhibiting spore germination. To elucidate the molecular basis of differential biocontrol abilities of Nagano and NCTC 7096, we compared GS production and biosurfactant secretion in addition to genome mining of the genomes. Our results proved that: (i) Using oil spreading, blood agar lysis, surface tension and tomato leaves wetness assays, Nagano showed increased biosurfactant secretion in comparison with NCTC 7096, (ii) Genome mining indicated the presence of GS genes in both Nagano and NCTC 7096 with two amino acid units difference between the strains: T342I and P419S. Using 3D models and the DUET server, T342I and P419S were predicted to decrease the stability of the NCTC 7096 GS synthase, (iii) Nagano produced two additional GS-like molecules GS-1155 (molecular weight 1155) and GS-1169 (molecular weight 1169), where one or two ornithine residues replace lysine in the peptide. There was also a negative correlation between surface tension and the quantity of GS-1169 present in Nagano, and (iv) the Nagano genome had a full protein network of exopolysaccharide biosynthesis in contrast to NCTC 7096 which lacked the first enzyme of the network. NCTC 7096 is unable to form biofilms as observed for Nagano. Different molecular layers, mainly gramicidin secondary metabolite production, account for differential biocontrol abilities of Nagano and NCTC 7096. This work highlighted the basis of differential biological control abilities between strains belonging to the same species and demonstrates techniques useful to the screening of effective biocontrol strains for environmentally friendly secondary metabolites that can be used to manage plant pathogens in the field.",
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note = "Acknowledgments This project was funded by the Government of Kuwait (to FA) and the European Union Seventh Framework Programme under grant agreement 245268 (ISEFOR; to LB and SW). Further support came from the SwissBOL project, financed by the Swiss Federal Office for the Environment (grant holder LB) and the Sciex–Scientific Exchange Programme (http://nms.ch/) (NMS.CH; to LL and LB). LL is indebted to the Ministry of Education, Science, Research and Sport of the Slovak Republic for financial support in the frame of the project “VEGA 1/0061/16” and “VEGA 1/0046/16”. Funding This project was funded by the Government of Kuwait (to FA) and the European Union Seventh Framework Programme under grant agreement 245268 (ISEFOR; to LB and SW). Further support came from the SwissBOL project, financed by the Swiss Federal Office for the Environment (grant holder LB) and the Sciex–Scientific Exchange Programme NMS.CH (to LL and LB). LL is indebted to the Ministry of Education, Science, Research and Sport of the Slovak Republic for financial support in the frame of the project “VEGA 1/0061/16.”",
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T1 - Increased Biological Activity of Aneurinibacillus migulanus Strains Correlates with the Production of New Gramicidin Secondary Metabolites

AU - Alenezi, Faizah N.

AU - Rekik, Imen

AU - Bouket, Ali Chenari

AU - Luptakova, Lenka

AU - Rateb, Mostafa E.

AU - Weitz, Hedda J.

AU - Jaspars, Marcel

AU - Woodward, Stephen

AU - Belbahri, Lassaad

N1 - Acknowledgments This project was funded by the Government of Kuwait (to FA) and the European Union Seventh Framework Programme under grant agreement 245268 (ISEFOR; to LB and SW). Further support came from the SwissBOL project, financed by the Swiss Federal Office for the Environment (grant holder LB) and the Sciex–Scientific Exchange Programme (http://nms.ch/) (NMS.CH; to LL and LB). LL is indebted to the Ministry of Education, Science, Research and Sport of the Slovak Republic for financial support in the frame of the project “VEGA 1/0061/16” and “VEGA 1/0046/16”. Funding This project was funded by the Government of Kuwait (to FA) and the European Union Seventh Framework Programme under grant agreement 245268 (ISEFOR; to LB and SW). Further support came from the SwissBOL project, financed by the Swiss Federal Office for the Environment (grant holder LB) and the Sciex–Scientific Exchange Programme NMS.CH (to LL and LB). LL is indebted to the Ministry of Education, Science, Research and Sport of the Slovak Republic for financial support in the frame of the project “VEGA 1/0061/16.”

PY - 2017/4/7

Y1 - 2017/4/7

N2 - The soil-borne gram-positive bacteria Aneurinibacillus migulanus strain Nagano shows considerable potential as a biocontrol agent against plant diseases. In contrast, A. migulanus NCTC 7096 proved less effective for inhibition of plant pathogens. Nagano strain exerts biocontrol activity against some gram-positive and gram-negative bacteria, fungi and oomycetes through the production of gramicidin S (GS). Apart from the antibiotic effects, GS increases the rate of evaporation from the plant surface, reducing periods of surface wetness and thereby indirectly inhibiting spore germination. To elucidate the molecular basis of differential biocontrol abilities of Nagano and NCTC 7096, we compared GS production and biosurfactant secretion in addition to genome mining of the genomes. Our results proved that: (i) Using oil spreading, blood agar lysis, surface tension and tomato leaves wetness assays, Nagano showed increased biosurfactant secretion in comparison with NCTC 7096, (ii) Genome mining indicated the presence of GS genes in both Nagano and NCTC 7096 with two amino acid units difference between the strains: T342I and P419S. Using 3D models and the DUET server, T342I and P419S were predicted to decrease the stability of the NCTC 7096 GS synthase, (iii) Nagano produced two additional GS-like molecules GS-1155 (molecular weight 1155) and GS-1169 (molecular weight 1169), where one or two ornithine residues replace lysine in the peptide. There was also a negative correlation between surface tension and the quantity of GS-1169 present in Nagano, and (iv) the Nagano genome had a full protein network of exopolysaccharide biosynthesis in contrast to NCTC 7096 which lacked the first enzyme of the network. NCTC 7096 is unable to form biofilms as observed for Nagano. Different molecular layers, mainly gramicidin secondary metabolite production, account for differential biocontrol abilities of Nagano and NCTC 7096. This work highlighted the basis of differential biological control abilities between strains belonging to the same species and demonstrates techniques useful to the screening of effective biocontrol strains for environmentally friendly secondary metabolites that can be used to manage plant pathogens in the field.

AB - The soil-borne gram-positive bacteria Aneurinibacillus migulanus strain Nagano shows considerable potential as a biocontrol agent against plant diseases. In contrast, A. migulanus NCTC 7096 proved less effective for inhibition of plant pathogens. Nagano strain exerts biocontrol activity against some gram-positive and gram-negative bacteria, fungi and oomycetes through the production of gramicidin S (GS). Apart from the antibiotic effects, GS increases the rate of evaporation from the plant surface, reducing periods of surface wetness and thereby indirectly inhibiting spore germination. To elucidate the molecular basis of differential biocontrol abilities of Nagano and NCTC 7096, we compared GS production and biosurfactant secretion in addition to genome mining of the genomes. Our results proved that: (i) Using oil spreading, blood agar lysis, surface tension and tomato leaves wetness assays, Nagano showed increased biosurfactant secretion in comparison with NCTC 7096, (ii) Genome mining indicated the presence of GS genes in both Nagano and NCTC 7096 with two amino acid units difference between the strains: T342I and P419S. Using 3D models and the DUET server, T342I and P419S were predicted to decrease the stability of the NCTC 7096 GS synthase, (iii) Nagano produced two additional GS-like molecules GS-1155 (molecular weight 1155) and GS-1169 (molecular weight 1169), where one or two ornithine residues replace lysine in the peptide. There was also a negative correlation between surface tension and the quantity of GS-1169 present in Nagano, and (iv) the Nagano genome had a full protein network of exopolysaccharide biosynthesis in contrast to NCTC 7096 which lacked the first enzyme of the network. NCTC 7096 is unable to form biofilms as observed for Nagano. Different molecular layers, mainly gramicidin secondary metabolite production, account for differential biocontrol abilities of Nagano and NCTC 7096. This work highlighted the basis of differential biological control abilities between strains belonging to the same species and demonstrates techniques useful to the screening of effective biocontrol strains for environmentally friendly secondary metabolites that can be used to manage plant pathogens in the field.

KW - secondary metabolism

KW - bioinformatics

KW - genome mining

KW - Aneurinibacillus migulanus

KW - Biocontrol bacteria

KW - Gramicidin S

KW - biosurfactant

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DO - 10.3389/fmicb.2017.00517

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VL - 8

SP - 1

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JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

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