Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp

Christina Victoria Viegelmann, Lekha Menon Margassery, Jonathan Kennedy, Tong Zhang, Ciarán O’Brien, Fergal O’Gara, John P. Morrissey, Alan D. W. Dobson, Ruangelie Edrada-Ebel

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

T Metabolomics and genomics are two complementary platforms for analyzing an organism as they provide information on the phenotype and genotype, respectively. These two techniques were applied in the dereplication and identification of bioactive compounds from a Streptomyces sp. (SM8) isolated from the sponge Haliclona simulans from Irish waters. Streptomyces strain SM8 extracts showed antibacterial and antifungal activity. NMR analysis of the active fractions proved that hydroxylated saturated fatty acids were the major components present in the antibacterial fractions. Antimycin compounds were initially putatively identified in the antifungal fractions using LC-Orbitrap. Their presence was later confirmed by comparison to a standard. Genomic analysis of
Streptomyces sp. SM8 revealed the presence of multiple secondary metabolism gene clusters, including a gene cluster for the biosynthesis of the antifungal antimycin family of compounds. The antimycin gene cluster of Streptomyces sp. SM8 was inactivated by disruption of the antimycin biosynthesis gene ant C. Extracts from this mutant strain showed loss of antimycin production and significantly less antifungal activity than the wild-type strain. Three butenolides, 4,10-dihydroxy-10-methyl-dodec-2-en-1,4-olide (1),4,11-dihydroxy-10-methyl-dodec-2-en-1,4-olide (2), and 4-hydroxy-10-methyl-11-oxo-dodec-2-en-1,4-olide(3) that had previously been reported from marine Streptomyces species were also isolated from SM8. Comparison of the extracts of Streptomyces strain SM8 and its host sponge, H. simulans, using LC-Orbitrap revealed the presence of metabolites common to both extracts, providing direct evidence linking sponge metabolites to a specific microbial symbiont.
LanguageEnglish
Pages3323-3351
Number of pages29
JournalMarine Drugs
Volume12
Issue number6
DOIs
Publication statusPublished - 2 Jun 2014

Fingerprint

Metabolomics
Streptomyces
Porifera
Multigene Family
Haliclona
Secondary Metabolism
Ants
Genomics
Fatty Acids
Genotype
antimycin
Phenotype
Water
Genes

Keywords

  • streptomyces
  • haliclona simulans
  • metabolomics
  • antimycin
  • antifungal
  • butenolide

Cite this

Viegelmann, C. V., Margassery, L. M., Kennedy, J., Zhang, T., O’Brien, C., O’Gara, F., ... Edrada-Ebel, R. (2014). Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp. Marine Drugs, 12(6), 3323-3351. https://doi.org/10.3390/md12063323
Viegelmann, Christina Victoria ; Margassery, Lekha Menon ; Kennedy, Jonathan ; Zhang, Tong ; O’Brien, Ciarán ; O’Gara, Fergal ; Morrissey, John P. ; Dobson, Alan D. W. ; Edrada-Ebel, Ruangelie. / Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp. In: Marine Drugs. 2014 ; Vol. 12, No. 6. pp. 3323-3351.
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Viegelmann, CV, Margassery, LM, Kennedy, J, Zhang, T, O’Brien, C, O’Gara, F, Morrissey, JP, Dobson, ADW & Edrada-Ebel, R 2014, 'Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp' Marine Drugs, vol. 12, no. 6, pp. 3323-3351. https://doi.org/10.3390/md12063323

Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp. / Viegelmann, Christina Victoria; Margassery, Lekha Menon ; Kennedy, Jonathan; Zhang, Tong; O’Brien, Ciarán ; O’Gara, Fergal ; Morrissey, John P.; Dobson, Alan D. W. ; Edrada-Ebel, Ruangelie.

In: Marine Drugs, Vol. 12, No. 6, 02.06.2014, p. 3323-3351.

Research output: Contribution to journalArticle

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T1 - Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp

AU - Viegelmann, Christina Victoria

AU - Margassery, Lekha Menon

AU - Kennedy, Jonathan

AU - Zhang, Tong

AU - O’Brien, Ciarán

AU - O’Gara, Fergal

AU - Morrissey, John P.

AU - Dobson, Alan D. W.

AU - Edrada-Ebel, Ruangelie

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N2 - T Metabolomics and genomics are two complementary platforms for analyzing an organism as they provide information on the phenotype and genotype, respectively. These two techniques were applied in the dereplication and identification of bioactive compounds from a Streptomyces sp. (SM8) isolated from the sponge Haliclona simulans from Irish waters. Streptomyces strain SM8 extracts showed antibacterial and antifungal activity. NMR analysis of the active fractions proved that hydroxylated saturated fatty acids were the major components present in the antibacterial fractions. Antimycin compounds were initially putatively identified in the antifungal fractions using LC-Orbitrap. Their presence was later confirmed by comparison to a standard. Genomic analysis ofStreptomyces sp. SM8 revealed the presence of multiple secondary metabolism gene clusters, including a gene cluster for the biosynthesis of the antifungal antimycin family of compounds. The antimycin gene cluster of Streptomyces sp. SM8 was inactivated by disruption of the antimycin biosynthesis gene ant C. Extracts from this mutant strain showed loss of antimycin production and significantly less antifungal activity than the wild-type strain. Three butenolides, 4,10-dihydroxy-10-methyl-dodec-2-en-1,4-olide (1),4,11-dihydroxy-10-methyl-dodec-2-en-1,4-olide (2), and 4-hydroxy-10-methyl-11-oxo-dodec-2-en-1,4-olide(3) that had previously been reported from marine Streptomyces species were also isolated from SM8. Comparison of the extracts of Streptomyces strain SM8 and its host sponge, H. simulans, using LC-Orbitrap revealed the presence of metabolites common to both extracts, providing direct evidence linking sponge metabolites to a specific microbial symbiont.

AB - T Metabolomics and genomics are two complementary platforms for analyzing an organism as they provide information on the phenotype and genotype, respectively. These two techniques were applied in the dereplication and identification of bioactive compounds from a Streptomyces sp. (SM8) isolated from the sponge Haliclona simulans from Irish waters. Streptomyces strain SM8 extracts showed antibacterial and antifungal activity. NMR analysis of the active fractions proved that hydroxylated saturated fatty acids were the major components present in the antibacterial fractions. Antimycin compounds were initially putatively identified in the antifungal fractions using LC-Orbitrap. Their presence was later confirmed by comparison to a standard. Genomic analysis ofStreptomyces sp. SM8 revealed the presence of multiple secondary metabolism gene clusters, including a gene cluster for the biosynthesis of the antifungal antimycin family of compounds. The antimycin gene cluster of Streptomyces sp. SM8 was inactivated by disruption of the antimycin biosynthesis gene ant C. Extracts from this mutant strain showed loss of antimycin production and significantly less antifungal activity than the wild-type strain. Three butenolides, 4,10-dihydroxy-10-methyl-dodec-2-en-1,4-olide (1),4,11-dihydroxy-10-methyl-dodec-2-en-1,4-olide (2), and 4-hydroxy-10-methyl-11-oxo-dodec-2-en-1,4-olide(3) that had previously been reported from marine Streptomyces species were also isolated from SM8. Comparison of the extracts of Streptomyces strain SM8 and its host sponge, H. simulans, using LC-Orbitrap revealed the presence of metabolites common to both extracts, providing direct evidence linking sponge metabolites to a specific microbial symbiont.

KW - streptomyces

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KW - antimycin

KW - antifungal

KW - butenolide

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Viegelmann CV, Margassery LM, Kennedy J, Zhang T, O’Brien C, O’Gara F et al. Metabolomic profiling and genomic study of a marine sponge-associated streptomyces sp. Marine Drugs. 2014 Jun 2;12(6):3323-3351. https://doi.org/10.3390/md12063323