Mining biosynthetic gene clusters in Virgibacillus genomes

Ghofran Othoum, Salim Bougouffa, Ameerah Bokhari, Feras F. Lafi, Takashi Gojobori, Heribert Hirt, Ivan Mijakovic, Vladimir B. Bajic, Magbubah Essack

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Abstract

Background: Biosynthetic gene clusters produce a wide range of metabolites with activities that are of interest to the pharmaceutical industry. Specific interest is shown towards those metabolites that exhibit antimicrobial activities against multidrug-resistant bacteria that have become a global health threat. Genera of the phylum Firmicutes are frequently identified as sources of such metabolites, but the biosynthetic potential of its Virgibacillus genus is not known. Here, we used comparative genomic analysis to determine whether Virgibacillus strains isolated from the Red Sea mangrove mud in Rabigh Harbor Lagoon, Saudi Arabia, may be an attractive source of such novel antimicrobial agents. Results: A comparative genomics analysis based on Virgibacillus dokdonensis Bac330, Virgibacillus sp. Bac332 and Virgibacillus halodenitrificans Bac324 (isolated from the Red Sea) and six other previously reported Virgibacillus strains was performed. Orthology analysis was used to determine the core genomes as well as the accessory genome of the nine Virgibacillus strains. The analysis shows that the Red Sea strain Virgibacillus sp. Bac332 has the highest number of unique genes and genomic islands compared to other genomes included in this study. Focusing on biosynthetic gene clusters, we show how marine isolates, including those from the Red Sea, are more enriched with nonribosomal peptides compared to the other Virgibacillus species. We also found that most nonribosomal peptide synthases identified in the Virgibacillus strains are part of genomic regions that are potentially horizontally transferred. Conclusions: The Red Sea Virgibacillus strains have a large number of biosynthetic genes in clusters that are not assigned to known products, indicating significant potential for the discovery of novel bioactive compounds. Also, having more modular synthetase units suggests that these strains are good candidates for experimental characterization of previously identified bioactive compounds as well. Future efforts will be directed towards establishing the properties of the potentially novel compounds encoded by the Red Sea specific trans-AT PKS/NRPS cluster and the type III PKS/NRPS cluster.
Original languageEnglish
Article number696
JournalBMC Genomics
Volume20
Issue number1
ISSN1471-2164
DOIs
Publication statusPublished - 2019

Cite this

Othoum, G., Bougouffa, S., Bokhari, A., Lafi, F. F., Gojobori, T., Hirt, H., ... Essack, M. (2019). Mining biosynthetic gene clusters in Virgibacillus genomes. BMC Genomics, 20(1), [696]. https://doi.org/10.1186/s12864-019-6065-7
Othoum, Ghofran ; Bougouffa, Salim ; Bokhari, Ameerah ; Lafi, Feras F. ; Gojobori, Takashi ; Hirt, Heribert ; Mijakovic, Ivan ; Bajic, Vladimir B. ; Essack, Magbubah. / Mining biosynthetic gene clusters in Virgibacillus genomes. In: BMC Genomics. 2019 ; Vol. 20, No. 1.
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title = "Mining biosynthetic gene clusters in Virgibacillus genomes",
abstract = "Background: Biosynthetic gene clusters produce a wide range of metabolites with activities that are of interest to the pharmaceutical industry. Specific interest is shown towards those metabolites that exhibit antimicrobial activities against multidrug-resistant bacteria that have become a global health threat. Genera of the phylum Firmicutes are frequently identified as sources of such metabolites, but the biosynthetic potential of its Virgibacillus genus is not known. Here, we used comparative genomic analysis to determine whether Virgibacillus strains isolated from the Red Sea mangrove mud in Rabigh Harbor Lagoon, Saudi Arabia, may be an attractive source of such novel antimicrobial agents. Results: A comparative genomics analysis based on Virgibacillus dokdonensis Bac330, Virgibacillus sp. Bac332 and Virgibacillus halodenitrificans Bac324 (isolated from the Red Sea) and six other previously reported Virgibacillus strains was performed. Orthology analysis was used to determine the core genomes as well as the accessory genome of the nine Virgibacillus strains. The analysis shows that the Red Sea strain Virgibacillus sp. Bac332 has the highest number of unique genes and genomic islands compared to other genomes included in this study. Focusing on biosynthetic gene clusters, we show how marine isolates, including those from the Red Sea, are more enriched with nonribosomal peptides compared to the other Virgibacillus species. We also found that most nonribosomal peptide synthases identified in the Virgibacillus strains are part of genomic regions that are potentially horizontally transferred. Conclusions: The Red Sea Virgibacillus strains have a large number of biosynthetic genes in clusters that are not assigned to known products, indicating significant potential for the discovery of novel bioactive compounds. Also, having more modular synthetase units suggests that these strains are good candidates for experimental characterization of previously identified bioactive compounds as well. Future efforts will be directed towards establishing the properties of the potentially novel compounds encoded by the Red Sea specific trans-AT PKS/NRPS cluster and the type III PKS/NRPS cluster.",
author = "Ghofran Othoum and Salim Bougouffa and Ameerah Bokhari and Lafi, {Feras F.} and Takashi Gojobori and Heribert Hirt and Ivan Mijakovic and Bajic, {Vladimir B.} and Magbubah Essack",
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Othoum, G, Bougouffa, S, Bokhari, A, Lafi, FF, Gojobori, T, Hirt, H, Mijakovic, I, Bajic, VB & Essack, M 2019, 'Mining biosynthetic gene clusters in Virgibacillus genomes', BMC Genomics, vol. 20, no. 1, 696. https://doi.org/10.1186/s12864-019-6065-7

Mining biosynthetic gene clusters in Virgibacillus genomes. / Othoum, Ghofran; Bougouffa, Salim; Bokhari, Ameerah; Lafi, Feras F.; Gojobori, Takashi; Hirt, Heribert; Mijakovic, Ivan; Bajic, Vladimir B.; Essack, Magbubah.

In: BMC Genomics, Vol. 20, No. 1, 696, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Mining biosynthetic gene clusters in Virgibacillus genomes

AU - Othoum, Ghofran

AU - Bougouffa, Salim

AU - Bokhari, Ameerah

AU - Lafi, Feras F.

AU - Gojobori, Takashi

AU - Hirt, Heribert

AU - Mijakovic, Ivan

AU - Bajic, Vladimir B.

AU - Essack, Magbubah

PY - 2019

Y1 - 2019

N2 - Background: Biosynthetic gene clusters produce a wide range of metabolites with activities that are of interest to the pharmaceutical industry. Specific interest is shown towards those metabolites that exhibit antimicrobial activities against multidrug-resistant bacteria that have become a global health threat. Genera of the phylum Firmicutes are frequently identified as sources of such metabolites, but the biosynthetic potential of its Virgibacillus genus is not known. Here, we used comparative genomic analysis to determine whether Virgibacillus strains isolated from the Red Sea mangrove mud in Rabigh Harbor Lagoon, Saudi Arabia, may be an attractive source of such novel antimicrobial agents. Results: A comparative genomics analysis based on Virgibacillus dokdonensis Bac330, Virgibacillus sp. Bac332 and Virgibacillus halodenitrificans Bac324 (isolated from the Red Sea) and six other previously reported Virgibacillus strains was performed. Orthology analysis was used to determine the core genomes as well as the accessory genome of the nine Virgibacillus strains. The analysis shows that the Red Sea strain Virgibacillus sp. Bac332 has the highest number of unique genes and genomic islands compared to other genomes included in this study. Focusing on biosynthetic gene clusters, we show how marine isolates, including those from the Red Sea, are more enriched with nonribosomal peptides compared to the other Virgibacillus species. We also found that most nonribosomal peptide synthases identified in the Virgibacillus strains are part of genomic regions that are potentially horizontally transferred. Conclusions: The Red Sea Virgibacillus strains have a large number of biosynthetic genes in clusters that are not assigned to known products, indicating significant potential for the discovery of novel bioactive compounds. Also, having more modular synthetase units suggests that these strains are good candidates for experimental characterization of previously identified bioactive compounds as well. Future efforts will be directed towards establishing the properties of the potentially novel compounds encoded by the Red Sea specific trans-AT PKS/NRPS cluster and the type III PKS/NRPS cluster.

AB - Background: Biosynthetic gene clusters produce a wide range of metabolites with activities that are of interest to the pharmaceutical industry. Specific interest is shown towards those metabolites that exhibit antimicrobial activities against multidrug-resistant bacteria that have become a global health threat. Genera of the phylum Firmicutes are frequently identified as sources of such metabolites, but the biosynthetic potential of its Virgibacillus genus is not known. Here, we used comparative genomic analysis to determine whether Virgibacillus strains isolated from the Red Sea mangrove mud in Rabigh Harbor Lagoon, Saudi Arabia, may be an attractive source of such novel antimicrobial agents. Results: A comparative genomics analysis based on Virgibacillus dokdonensis Bac330, Virgibacillus sp. Bac332 and Virgibacillus halodenitrificans Bac324 (isolated from the Red Sea) and six other previously reported Virgibacillus strains was performed. Orthology analysis was used to determine the core genomes as well as the accessory genome of the nine Virgibacillus strains. The analysis shows that the Red Sea strain Virgibacillus sp. Bac332 has the highest number of unique genes and genomic islands compared to other genomes included in this study. Focusing on biosynthetic gene clusters, we show how marine isolates, including those from the Red Sea, are more enriched with nonribosomal peptides compared to the other Virgibacillus species. We also found that most nonribosomal peptide synthases identified in the Virgibacillus strains are part of genomic regions that are potentially horizontally transferred. Conclusions: The Red Sea Virgibacillus strains have a large number of biosynthetic genes in clusters that are not assigned to known products, indicating significant potential for the discovery of novel bioactive compounds. Also, having more modular synthetase units suggests that these strains are good candidates for experimental characterization of previously identified bioactive compounds as well. Future efforts will be directed towards establishing the properties of the potentially novel compounds encoded by the Red Sea specific trans-AT PKS/NRPS cluster and the type III PKS/NRPS cluster.

U2 - 10.1186/s12864-019-6065-7

DO - 10.1186/s12864-019-6065-7

M3 - Journal article

VL - 20

JO - B M C Genomics

JF - B M C Genomics

SN - 1471-2164

IS - 1

M1 - 696

ER -

Othoum G, Bougouffa S, Bokhari A, Lafi FF, Gojobori T, Hirt H et al. Mining biosynthetic gene clusters in Virgibacillus genomes. BMC Genomics. 2019;20(1). 696. https://doi.org/10.1186/s12864-019-6065-7