Dynamics of the compartmentalized Streptomyces chromosome during metabolic differentiation

Lioy, Virginia S.; Lorenzi, Jean-Noël; Najah, Soumaya; Poinsignon, Thibault; Leh, Hervé; Saulnier, Corinne; Aigle, Bertrand; Lautru, Sylvie; Thibessard, Annabelle; Lespinet, Olivier; Leblond, Pierre; Jaszczyszyn, Yan; Gorrichon, Kévin; Varoquaux, Nelle; Junier, Ivan; Boccard, Frédéric; Pernodet, Jean‐Luc; Bury‐Moné, Stéphanie

doi:10.21203/rs.3.rs-145840/v1

Cited by 4 publications

(23 citation statements)

References 61 publications

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“…We first characterized the organization of rrn operons in 127 Streptomyces genomes from a previously characterized panel of Streptomyces species representative of the genus diversity (Lorenzi et al 2021; Virginia S. Lioy et al 2021) ( Supplemental Table S1 ). In this panel, most genomes (>85 %) share an average nucleotide identity based on BLAST+ (ANIb) lower than 95 %, a threshold used to distinguish species (Richter et Rosselló-Móra 2009) ( Supplemental Table S2 ).…”

Section: Resultsmentioning

confidence: 99%

“…Although 16S RNA sequences are the classical ‘chronometer’ for phylogenetic classification, their impact on genome evolution per se has rarely been considered (Espejo et Plaza 2018). Interestingly, the rrn operons, including 16S, 23S, 5S and internal transcribed spacer regions, coincide with sharp boundaries in the chromosome 3D-organization of bacteria with linear (Virginia S. Lioy et al 2021) as well as circular (V. S. Lioy et al 2018; Le et Laub 2016; Böhm et al 2020; Marbouty et al 2015; Wang et al 2015) genomes. The formation of these boundaries correlates with a very high level of transcription, but does not require translation (Le et Laub 2016).…”

Section: Introductionmentioning

confidence: 94%

“…Their genome is amongst the largest in bacteria (6-15 Mb), with an extreme GC content (circa 72%). In addition, the Streptomyces chromosome presents a partition, termed ‘genetic compartmentalization’, into a core region harboring genes shared by all Streptomyces and more variable extremities or ‘arms’ enriched in specialized metabolite biosynthetic gene clusters (Redenbach et al 1996; Omura et al 2001; Karoonuthaisiri et al 2005; Ikeda et al 2003; Choulet et al 2006; Bentley et al 2002; Lorenzi et al 2021; Virginia S. Lioy et al 2021). Consistently, DNA rearrangements and recombination events are more frequently fixed in the terminal arms than in the central region (Choulet et al 2006; Fischer et al 1998; Hoff et al 2018; Tidjani et al 2019; Hopwood 2006; Zhang et al 2020).…”

Section: Introductionmentioning

confidence: 99%

“…We recently demonstrated that the genetic compartmentalization of Streptomyces ambofaciens ATCC 23877 correlates with chromosome architecture and gene expression in exponential phase (Virginia S. Lioy et al 2021). During vegetative growth, the distal ribosomal RNA ( rrn ) operons delimit a highly structured and expressed region termed ‘central compartment’, presenting structural features distinct from those of the terminal compartments which are almost transcriptionally quiescent (Virginia S. Lioy et al 2021). This led us to propose that these distal rrn operons may constitute some kind of barrier contributing to the evolution of Streptomyces genomes towards a compartmentalized organization (Virginia S. Lioy et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…During vegetative growth, the distal ribosomal RNA ( rrn ) operons delimit a highly structured and expressed region termed ‘central compartment’, presenting structural features distinct from those of the terminal compartments which are almost transcriptionally quiescent (Virginia S. Lioy et al 2021). This led us to propose that these distal rrn operons may constitute some kind of barrier contributing to the evolution of Streptomyces genomes towards a compartmentalized organization (Virginia S. Lioy et al 2021).…”

Section: Introductionmentioning

confidence: 99%

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Ribosomal RNA operons define a central functional compartment in the Streptomyces chromosome

Lorenzi

Thibessard

Lioy

et al. 2022

Preprint

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Streptomyces are prolific producers of specialized metabolites with applications in medicine and agriculture. These bacteria possess a large linear chromosome genetically compartmentalized: core genes are grouped in the central part, while terminal regions are populated by poorly conserved genes and define the chromosomal arms. In exponentially growing cells, chromosome conformation capture unveiled sharp boundaries formed by ribosomal RNA (rrn) operons that segment the chromosome into multiple domains. The first and last rrn operons delimit the highly expressed central compartment and the rather transcriptionally silent terminal compartments. Here we further explore the link between the genetic distribution of rrn operons and Streptomyces genomic compartmentalization. A large panel of genomes of species representative of the genus diversity revealed that rrn operons and core genes form a central skeleton, the former being identifiable from their core gene environment. We implemented a new nomenclature for Streptomyces genomes and trace their rrn-based evolutionary history. Remarkably, rrn operons are close to pericentric inversions. Moreover, the central compartment delimited by rrn operons has a very dense, nearly invariant core gene content. Finally, this compartment harbors genes with the highest expression levels, regardless of gene persistence and distance to the origin of replication. Our results highlight that rrn operons define the structural boundaries of a central functional compartment prone to transcription in Streptomyces.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Ribosomal RNA operons define a central functional compartment in the Streptomyces chromosome

Lorenzi

Thibessard

Lioy

et al. 2022

Preprint

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Genomic adaptation in the CAZyome and specialised metabolism of the plant-associated Streptomyces violaceusniger clade

Gayrard

Veyssière

Adam

et al. 2021

Preprint

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Streptomycetes are Gram-positive actinobacteria largely represented in the plant root microbiota. The genetic determinants involved in the presence of Streptomyces in the rhizosphere are largely unknown and can rely on the ability to degrade plant-derived compounds such as cell-wall polysaccharides and on the production of specialised metabolites. To address whether Streptomyces strains recruited into root microbiota share genomic specificities related to these two functions, we engaged a comparative genomic analysis using a newly sequenced rhizospheric strain, Streptomyces sp. AgN23 and strains from the phylogenetically related S. violaceusniger clade. This analysis enlightens a shared prominent CAZyome potentially involved in plant polysaccharides degradation and a strong conservation of antimicrobials biosynthetic clusters (rustmicin, mediomycin, niphimycin, nigericin) as well as plant bioactive compounds (nigericin, echosides, elaiophylin). Taken together, our work supports the hypothesis that specific hydrolytic enzymes and specialised metabolites repertoires may play important roles in the development of Streptomyces strains in the rhizosphere.

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Transcriptional Regulation of Congocidine (Netropsin) Biosynthesis and Resistance

Vingadassalon

Lorieux

Juguet

et al. 2021

Appl Environ Microbiol

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The production of specialized metabolites by Streptomyces bacteria is usually temporally regulated. This regulation is complex and frequently involves both global and pathway-specific mechanisms. Streptomyces ambofaciens ATCC23877 produces several specialized metabolites, including spiramycins, stambomycins, kinamycins and congocidine. The production of the first three molecules has been shown to be controlled by one or several cluster-situated transcriptional regulators. However, nothing is known regarding the regulation of congocidine biosynthesis. Congocidine (netropsin) belongs to the family of pyrrolamide metabolites, which also includes distamycin and anthelvencins. Most pyrrolamides bind into the minor groove of DNA, specifically in A/T-rich regions, which gives them numerous biological activities, such as antimicrobial and antitumoral activities. We previously reported the characterization of the pyrrolamide biosynthetic gene clusters of congocidine ( cgc ) in S. ambofaciens ATCC23877, distamycin ( dst ) in Streptomyces netropsis DSM40846 and anthelvencins ( ant ) in Streptomyces venezuelae ATCC14583. The three gene clusters contain a gene encoding a putative transcriptional regulator, cgc1 , dst1 and ant1 respectively. Cgc1, Dst1 and Ant1 present a high percentage of amino acid sequence similarity. We demonstrate here that Cgc1, an atypical orphan response regulator, activates the transcription of all cgc genes in the stationary phase of S. ambofaciens growth. We also show that the cgc cluster is constituted of eight main transcriptional units. Finally, we show that congocidine induces the expression of the transcriptional regulator Cgc1 and of the operon containing the resistance genes ( cgc20 and cgc21 , coding for an ABC transporter), and propose a model for the transcriptional regulation of the cgc gene cluster. Importance Understanding the mechanisms of regulation of specialized metabolite production can have important implications both at the level of specialized metabolism study (expression of silent gene clusters) and the biotechnological level (increase of the production of a metabolite of interest). We report here a study on the regulation of the biosynthesis of a metabolite from the pyrrolamide family, congocidine. We show that congocidine biosynthesis and resistance is controlled by Cgc1, a cluster-situated regulator. As the gene clusters directing the biosynthesis of the pyrrolamides distamycin and anthelvencin encode a homolog of Cgc1, our findings may be relevant for the biosynthesis of other pyrrolamides. In addition, our results reveal a new type of feed-forward induction mechanism, in which congocidine induces its own biosynthesis through the induction of the transcription of cgc1 .

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Dynamics of the compartmentalized Streptomyces chromosome during metabolic differentiation

Cited by 4 publications

References 61 publications

Ribosomal RNA operons define a central functional compartment in the Streptomyces chromosome

Ribosomal RNA operons define a central functional compartment in the Streptomyces chromosome

Genomic adaptation in the CAZyome and specialised metabolism of the plant-associated Streptomyces violaceusniger clade

Transcriptional Regulation of Congocidine (Netropsin) Biosynthesis and Resistance

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