Biological Impact of a Large Scale Genomic Inversion that Grossly Disrupts the Relative Positions of the Origin and Terminus Loci of the Streptococcus pyogenes Chromosome

Savic, Dragutin J.; Nguyen, Scott V.; McCullor, Kimberly A.; McShan, W. Michael

doi:10.1101/534933

Cited by 2 publications

(2 citation statements)

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“…Increasing evidence suggests that gene order within the bacterial chromosome contributes to cellular homeostasis by coordinating key entangled processes such as chromosome structuration, cell cycle, replication and the expression of genetic information. While genome reshuffling experiments have not been yet performed in bacterial systems (79) approaches such as comparative genomics (17,18,21,23,31,80), systems biology (20), large DNA inversions (81)(82)(83) and relocation of individual gene sets (16,19,(84)(85)(86) have provided support to this notion. Genes encoding for the genetic information flow are interesting models to test the role of genomic position on cellular physiology.…”

Section: Discussionmentioning

confidence: 99%

Chromosomal position of ribosomal protein genes impacts long term evolution ofVibrio cholerae

Mornico

Bernal-Bayard

Ghigo

et al. 2022

Preprint

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It is unclear how gene order within the chromosome influences bacterial evolution. The genomic location of genes encoding the flow of genetic information is biased towards the replication origin (oriC) in fast-growing bacteria. To study the role of chromosomal location on cell physiology we relocated the S10-spec-α locus (S10), harboring half of ribosomal protein genes, to different chromosomal positions in the fast-growing pathogen V. cholerae. We found that growth rate, fitness and infectivity inversely correlated the distance between S10 and oriC. To gain insight into the evolutionary effect of RP genomic position, we evolved strains bearing S10 at its current oriC-proximal location or derivatives harboring the locus far from it (i.e. 1.5Mbp). Populations deep sequencing on average 1 mutation fixed each 100 generations, mainly at genes linked to flagellum regulation, lipopolysaccharide synthesis, chemotaxis, biofilm and quorum sensing. Along the experiment, populations showed an increment in biofilm forming capacity. All populations increased their growth rate. However, growth rate advantage of populations bearing S10 at an oriC-proximal persisted along the experiment over those where the main ribosomal protein gene cluster locates at an oriC-distal position. This indicates that suppressor mutations cannot compensate S10 genomic location. We selected fast-growing clones displaying a ∼10% growth rate increment finding that they harbored inactivating mutations at, among other sites, flagellum master regulators flrAB regardless S10 genomic location. The introduction of these mutations on naïve V. cholerae strains resulted in a ∼10% increase in growth rate. Our study therefore demonstrates that the location of ribosomal protein genes conditions the evolutionary trajectory of growth rate in the long term. While genomic content is highly plastic in prokaryotes, gene order is an underestimated factor that conditions cellular physiology and lineage evolution. The lack of suppression enables artificial gene relocation for genetic circuit reprogramming.

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Section: Discussionmentioning

confidence: 99%

Chromosomal position of ribosomal protein genes impacts long term evolution ofVibrio cholerae

Mornico

Bernal-Bayard

Ghigo

et al. 2022

Preprint

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“…Orthogonal techniques are required to identify this class of mutations. Those are either laborious molecular methods such as PFGE or optical mapping of restriction-endonuclease-digested genomic DNA followed by site-specific PCR covering the breakpoints of the inversion for validation [14,15], or long-read sequencing that incurs a significant extra cost [11]. Therefore, the effect of chromosomal inversions on bacterial physiology has often been overlooked in bacterial evolution studies due to the failure to detect the inversion with short-read sequencing alone.…”

Section: Introductionmentioning

confidence: 99%

A large chromosomal inversion affects antimicrobial sensitivity of Escherichia coli to sodium deoxycholate

León-Quezada

Biggs

et al. 2022

Microbiology

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Resistance to antimicrobials is normally caused by mutations in the drug targets or genes involved in antimicrobial activation or expulsion. Here we show that an Escherichia coli strain, named DOC14, selected for increased resistance to the bile salt sodium deoxycholate, has no mutations in any ORF, but instead has a 2.1 Mb chromosomal inversion. The breakpoints of the inversion are two inverted copies of an IS5 element. Besides lowering deoxycholate susceptibility, the IS5-mediated chromosomal inversion in the DOC14 mutant was found to increase bacterial survival upon exposure to ampicillin and vancomycin, and sensitize the cell to ciprofloxacin and meropenem, but does not affect bacterial growth or cell morphology in a rich medium in the absence of antibacterial molecules. Overall, our findings support the notion that a large chromosomal inversion can benefit bacterial cells under certain conditions, contributing to genetic variability available for selection during evolution. The DOC14 mutant paired with its isogenic parental strain form a useful model as bacterial ancestors in evolution experiments to study how a large chromosomal inversion influences the evolutionary trajectory in response to various environmental stressors.

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Biological Impact of a Large Scale Genomic Inversion that Grossly Disrupts the Relative Positions of the Origin and Terminus Loci of the Streptococcus pyogenes Chromosome

Cited by 2 publications

References 61 publications

Chromosomal position of ribosomal protein genes impacts long term evolution ofVibrio cholerae

Chromosomal position of ribosomal protein genes impacts long term evolution ofVibrio cholerae

A large chromosomal inversion affects antimicrobial sensitivity of Escherichia coli to sodium deoxycholate

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