Unprecedented large inverted repeats at the replication terminus of circular bacterial chromosomes suggest a novel mode of chromosome rescue

Kafsi, Hela El; Loux, Valentin; Mariadassou, Mahendra; Blin, Camille; Chiapello, Hélène; Abraham, Anne-Laure; Maguin, Emmanuelle; Guchte, Maarten van de

doi:10.1038/srep44331

Cited by 7 publications

(8 citation statements)

References 44 publications

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“…Evidence for fold-back inversions has been found in the genomes of viruses (28), prokaryotes (29), is associated with genetic disease (22,30,31) and a variety of cancers (32-34) Moreover, fold-back inversions observed in human cancer cells having escaped telomere-driven crisis occur independently of DSB repair (35,36), consistent with our findings. Thus, we anticipate that this study will contribute to the understanding of rapid genome evolution, pathogenesis and tumorigenesis.…”

supporting

confidence: 90%

Persistent broken chromosome inheritance drives genome instability

Pai

Durley

Cheng

et al. 2020

Preprint

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Persistent DNA damage arising from unrepaired broken chromosomes or telomere loss can promote DNA damage checkpoint adaptation, and cell cycle progression, thereby increasing cell survival but also genome instability. However, the nature and extent of such instability is unclear. We show, using Schizosaccharomyces pombe, that inherited broken chromosomes, arising from failed homologous recombination repair, are subject to cycles of segregation, DNA replication and extensive end-processing, termed here SERPent cycles, by daughter cells, over multiple generations. Following Chk1 loss these post-adaptive cycles continue until extensive processing through inverted repeats promotes annealing, fold-back inversion and a spectrum of chromosomal rearrangements, typically isochromosomes, or chromosome loss, in the resultant population. These findings explain how persistent DNA damage drives widespread genome instability, with implications for punctuated evolution, genetic disease and tumorigenesis.One Sentence SummaryReplication and processing of inherited broken chromosomes drives chromosomal instability.

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supporting

confidence: 90%

Persistent broken chromosome inheritance drives genome instability

Pai

Durley

Cheng

et al. 2020

Preprint

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“…The natural occurrence of long inverted repeats close to the replication termination site in bacteria with circular chromosomes appears to be rare, based on a recent analysis of 1373 sequenced genomes [ 40 ]. According to the authors, among bacteria that had not been manipulated artificially, this property was found only in the branch of Lactobacillus delbrueckii designated subsp .…”

Section: Discussionmentioning

confidence: 99%

“…The most intriguing features of this strain are the large size of the repeats (553 kb, versus only 38 kb in L. delbrueckii subsp . bulgaricus [ 40 ]) for each copy of the duplicated region, and the loss of its natural replication termination machinery, for which the dif and xerCD genes were probably the most important elements [ 32 ]. The aforementioned analysis of 1373 genomes [ 40 ] dealt only with deposited assemblies and not with raw sequencing data.…”

Section: Discussionmentioning

confidence: 99%

“…bulgaricus [ 40 ]) for each copy of the duplicated region, and the loss of its natural replication termination machinery, for which the dif and xerCD genes were probably the most important elements [ 32 ]. The aforementioned analysis of 1373 genomes [ 40 ] dealt only with deposited assemblies and not with raw sequencing data. We investigated the B. thuringiensis and B. cereus genomes further, by applying a read alignment protocol to a set of 91 raw sequencing reads for B. thuringiensis and 480 for B. cereus , using the B. thuringiensis serovar israelensis AM65-52 chromosome as the alignment template.…”

Section: Discussionmentioning

confidence: 99%

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Long inverted repeats around the chromosome replication terminus in the model strain Bacillus thuringiensis serovar israelensis BGSC 4Q7

et al. 2020

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Bacillus thuringiensis serovar israelensis is the most widely used natural biopesticide against mosquito larvae worldwide. Its lineage has been actively studied and a plasmid-free strain, B . thuringiensis serovar israelensis BGSC 4Q7 (4Q7), has been produced. Previous sequencing of the genome of this strain has revealed the persistent presence of a 235 kb extrachromosomal element, pBtic235, which has been shown to be an inducible prophage, although three putative chromosomal prophages have been lost. Moreover, a 492 kb region, potentially including the standard replication terminus, has also been deleted in the 4Q7 strain, indicating an absence of essential genes in this area. We reanalysed the genome coverage distribution of reads for the previously sequenced variant strain, and sequenced two independently maintained samples of the 4Q7 strain. A 553 kb area, close to the 492 kb deletion, was found to be duplicated. This duplication presumably restored the equal sizes of the replichores, and a balanced functioning of replication termination. An analysis of genome assembly graphs revealed a transient association of the host chromosome with the pBtic235 element. This association may play a functional role in the replication of the bacterial chromosome, and the termination of this process in particular. The genome-restructuring events detected may modify the genetic status of cytotoxic or haemolytic toxins, potentially influencing strain virulence. Twelve of the single-nucleotide variants identified in 4Q7 were probably due to the procedure used for strain construction or were present in the precursor of this strain. No sequence variants were found in pBtic235, but the distribution of the corresponding 4Q7 reads indicates a significant difference from counterparts in natural B. thuringiensis serovar israelensis strains, suggesting a duplication or over-replication in 4Q7. Thus, the 4Q7 strain is not a pure plasmid-less offshoot, but a highly genetically modified derivative of its natural ancestor. In addition to potentially influencing virulence, genome-restructuring events can modify the replication termination machinery. These findings have potential implications for the conclusions of virulence studies on 4Q7 as a model, but they also raise interesting fundamental questions about the functioning of the Bacillus genome.

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“…Transposable elements often contain genes of interest encoding traits such as antibiotic resistance and bacteriocin production (Klaenhammer, 1993;Toomey et al, 2009). In some cases, critical processes such as genome replication are also intrinsically linked to the presence of inverted repeats (El Kafsi et al, 2017) and structure variants of large genomic transfers between species often harbor crucial mechanisms (Kant et al, 2011). Progress in this area will have a significant impact on determining some of the poorly understood traits associated with LAB (Teusink and Molenaar, 2017).…”

Section: The Impact Of Genomics On Lactic Acid Bacteriamentioning

confidence: 99%

The Progress of Multi-Omics Technologies: Determining Function in Lactic Acid Bacteria Using a Systems Level Approach

2020

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Lactic Acid Bacteria (LAB) have long been recognized as having a significant impact ranging from commercial to health domains. A vast amount of research has been carried out on these microbes, deciphering many of the pathways and components responsible for these desirable effects. However, a large proportion of this functional information has been derived from a reductionist approach working with pure culture strains. This provides limited insight into understanding the impact of LAB within intricate systems such as the gut microbiome or multi strain starter cultures. Whole genome sequencing of strains and shotgun metagenomics of entire systems are powerful techniques that are currently widely used to decipher function in microbes, but they also have their limitations. An available genome or metagenome can provide an image of what a strain or microbiome, respectively, is potentially capable of and the functions that they may carry out. A top-down, multi-omics approach has the power to resolve the functional potential of an ecosystem into an image of what is being expressed, translated and produced. With this image, it is possible to see the real functions that members of a system are performing and allow more accurate and impactful predictions of the effects of these microorganisms. This review will discuss how technological advances have the potential to increase the yield of information from genomics, transcriptomics, proteomics and metabolomics. The potential for integrated omics to resolve the role of LAB in complex systems will also be assessed. Finally, the current software approaches for managing these omics data sets will be discussed.

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Unprecedented large inverted repeats at the replication terminus of circular bacterial chromosomes suggest a novel mode of chromosome rescue

Cited by 7 publications

References 44 publications

Persistent broken chromosome inheritance drives genome instability

Persistent broken chromosome inheritance drives genome instability

Long inverted repeats around the chromosome replication terminus in the model strain Bacillus thuringiensis serovar israelensis BGSC 4Q7

The Progress of Multi-Omics Technologies: Determining Function in Lactic Acid Bacteria Using a Systems Level Approach

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