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The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island

The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island
The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island

The complete genome sequence of the original isolate of the model actinomycete Streptomyces lividans 66, also referred to as 1326, was deciphered after a combination of next-generation sequencing platforms and a hybrid assembly pipeline. Comparative analysis of the genomes of S. lividans 66 and closely related strains, including S. coelicolor M145 and S. lividans TK24, was used to identify strain-specific genes. The genetic diversity identified included a large genomic island with a mosaic structure, present in S. lividans 66 but not in the strain TK24. Sequence analyses showed that this genomic island has an anomalous (G +C) content, suggesting recent acquisition and that it is rich in metal-related genes. Sequences previously linked to a mobile conjugative element, termed plasmid SLP3 and defined here as a 94 kb region, could also be identified within this locus. Transcriptional analysis of the response of S. lividans 66 to copper was used to corroborate a role of this large genomic island, including two SLP3-borne "cryptic" peptide biosynthetic gene clusters, in metal homeostasis. Notably, one of these predicted biosynthetic systems includes an unprecedented nonribosomal peptide synthetase-tRNA-dependent transferase biosynthetic hybrid organization. This observation implies the recruitment of members of the leucyl/phenylalanyl-tRNA-protein transferase family to catalyze peptide bond formation within the biosynthesis of natural products. Thus, the genome sequence of S. lividans 66 not only explains long-standing genetic and phenotypic differences but also opens the door for further in-depth comparative genomic analyses of model Streptomyces strains, as well as for the discovery of novel natural products following genome-mining approaches.

Bacterial next-generation genome sequencing, Copper homeostasis, L/F trna transferase, Peptide biosynthesis, Streptomyces comparative genomics
1759-6653
1165-1175
Cruz-Morales, Pablo
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Vijgenboom, Erik
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Iruegas-Bocardo, Fernanda
cd173072-ca61-498d-908c-8bc70fdda4ac
Girard, Geneviève
052608ad-702b-4cfe-88c6-ddcc2229d20d
Yáñez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Ramos-Aboites, Hilda E.
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Pernodet, Jean Luc
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Anné, Jozef
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Van Wezel, Gilles P.
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Barona-Gómez, Francisco
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Cruz-Morales, Pablo
75d96b74-68e4-4550-9020-286a0d9dd2f3
Vijgenboom, Erik
46d04660-9dc1-40e1-8a4a-71986a7bae0d
Iruegas-Bocardo, Fernanda
cd173072-ca61-498d-908c-8bc70fdda4ac
Girard, Geneviève
052608ad-702b-4cfe-88c6-ddcc2229d20d
Yáñez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Ramos-Aboites, Hilda E.
67ff75d0-69f3-46c7-be85-7115b51d7d50
Pernodet, Jean Luc
5b208e7a-f82e-492e-9196-4e6afee94ce7
Anné, Jozef
e0ed0709-8dc4-4075-8a97-03fa552767e2
Van Wezel, Gilles P.
83cccd0e-dcfb-42c9-bbc7-3478b863cd05
Barona-Gómez, Francisco
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Cruz-Morales, Pablo, Vijgenboom, Erik, Iruegas-Bocardo, Fernanda, Girard, Geneviève, Yáñez-Guerra, Luis Alfonso, Ramos-Aboites, Hilda E., Pernodet, Jean Luc, Anné, Jozef, Van Wezel, Gilles P. and Barona-Gómez, Francisco (2013) The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biology and Evolution, 5 (6), 1165-1175. (doi:10.1093/gbe/evt082).

Record type: Article

Abstract

The complete genome sequence of the original isolate of the model actinomycete Streptomyces lividans 66, also referred to as 1326, was deciphered after a combination of next-generation sequencing platforms and a hybrid assembly pipeline. Comparative analysis of the genomes of S. lividans 66 and closely related strains, including S. coelicolor M145 and S. lividans TK24, was used to identify strain-specific genes. The genetic diversity identified included a large genomic island with a mosaic structure, present in S. lividans 66 but not in the strain TK24. Sequence analyses showed that this genomic island has an anomalous (G +C) content, suggesting recent acquisition and that it is rich in metal-related genes. Sequences previously linked to a mobile conjugative element, termed plasmid SLP3 and defined here as a 94 kb region, could also be identified within this locus. Transcriptional analysis of the response of S. lividans 66 to copper was used to corroborate a role of this large genomic island, including two SLP3-borne "cryptic" peptide biosynthetic gene clusters, in metal homeostasis. Notably, one of these predicted biosynthetic systems includes an unprecedented nonribosomal peptide synthetase-tRNA-dependent transferase biosynthetic hybrid organization. This observation implies the recruitment of members of the leucyl/phenylalanyl-tRNA-protein transferase family to catalyze peptide bond formation within the biosynthesis of natural products. Thus, the genome sequence of S. lividans 66 not only explains long-standing genetic and phenotypic differences but also opens the door for further in-depth comparative genomic analyses of model Streptomyces strains, as well as for the discovery of novel natural products following genome-mining approaches.

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More information

Published date: June 2013
Keywords: Bacterial next-generation genome sequencing, Copper homeostasis, L/F trna transferase, Peptide biosynthesis, Streptomyces comparative genomics

Identifiers

Local EPrints ID: 483500
URI: http://eprints.soton.ac.uk/id/eprint/483500
ISSN: 1759-6653
PURE UUID: 6885ce28-9346-4c1f-9408-961c3fe6d96c
ORCID for Luis Alfonso Yáñez-Guerra: ORCID iD orcid.org/0000-0002-2523-1310

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Date deposited: 31 Oct 2023 18:24
Last modified: 18 Mar 2024 04:15

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Contributors

Author: Pablo Cruz-Morales
Author: Erik Vijgenboom
Author: Fernanda Iruegas-Bocardo
Author: Geneviève Girard
Author: Luis Alfonso Yáñez-Guerra ORCID iD
Author: Hilda E. Ramos-Aboites
Author: Jean Luc Pernodet
Author: Jozef Anné
Author: Gilles P. Van Wezel
Author: Francisco Barona-Gómez

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