Coevolution of the Organization and Structure of Prokaryotic Genomes

Touchon, Marie; Rocha, Eduardo P. C.

doi:10.1101/cshperspect.a018168

Cited by 59 publications

(78 citation statements)

References 182 publications

(175 reference statements)

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“…2C). The distribution of genes on the leading and lagging strand further supports this model: in line with expectations(Touchon and Rocha 2016;Hao and Golding 2009), the majority of Topology of HGT into the GPA clade. (A) Density profiles illustrating the relative enrichment/depletion of HT(green/red) and vertical (yellow) genes across length-normalized GPA genomes.…”

supporting

confidence: 74%

Horizontal gene flow into Geobacillus is constrained by the chromosomal organization of growth and sporulation

Esin

Ellis

Warnecke

2018

Preprint

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Horizontal gene transfer (HGT) in bacteria occurs in the context of adaptive genome architecture. As a consequence, some chromosomal neighbourhoods are likely more permissive to HGT than others. Here, we investigate the chromosomal topology of horizontal gene flow into a clade of Bacillaceae that includes Geobacillus spp. Reconstructing HGT patterns using a phylogenetic approach coupled to model-based reconciliation, we discover three large contiguous chromosomal zones of HGT enrichment. These zones encompass and connect classically defined genomic islands. Analyzing topological and strand biases of recent and older transfer events, we show that restrictions on entry are rapidly enforced by selection and that restrictive and permissive zones have existed in their current locations for long periods of evolution. The largest zone, characterized by a high influx of metabolic genes, is centred on the terminus. The other two zones flank a narrow non-permissive zone around the origin of replication and extend to delimit the first third of the chromosome -the part of the chromosome that is confined to the forespore during early spore formation.Horizontal transfers into this area are biased towards functions classically controlled by the forespore-specific sigma factor σ F : signal transduction, transcription, and particularly membrane biogenesis. Similar enrichment patterns are present in spore-forming but absent in non-spore-forming Bacilli. Our results suggest that the topology of HGT in Geobacillus, and Bacilli more generally, reflects constraints imposed by chromosomal organization for fast and sporulation, as asymmetric chromosomal entrapment in the forespore during early spore formation restricts where HGT-driven innovation in sporulation can occur.

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supporting

confidence: 74%

Horizontal gene flow into Geobacillus is constrained by the chromosomal organization of growth and sporulation

Esin

Ellis

Warnecke

2018

Preprint

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“…While higher-level functional clustering in bacterial genomes has been reported previously143233343536, these structures have so far not been linked to HGT. Future studies on the properties and the evolution of SOCs may greatly contribute to our understanding of the structure and evolutionary dynamics of prokaryotic genomes.…”

Section: Discussionmentioning

confidence: 71%

Supra-operonic clusters of functionally related genes (SOCs) are a source of horizontal gene co-transfers

Pang

Lercher

2017

Sci Rep

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Adaptation of bacteria occurs predominantly via horizontal gene transfer (HGT). While it is widely recognized that horizontal acquisitions frequently encompass multiple genes, it is unclear what the size distribution of successfully transferred DNA segments looks like and what evolutionary forces shape this distribution. Here, we identified 1790 gene family pairs that were consistently co-gained on the same branches across a phylogeny of 53 E. coli strains. We estimated a lower limit of their genomic distances at the time they were transferred to their host genomes; this distribution shows a sharp upper bound at 30 kb. The same gene-pairs can have larger distances (up to 70 kb) in other genomes. These more distant pairs likely represent recent acquisitions via transduction that involve the co-transfer of excised prophage genes, as they are almost always associated with intervening phage-associated genes. The observed distribution of genomic distances of co-transferred genes is much broader than expected from a model based on the co-transfer of genes within operons; instead, this distribution is highly consistent with the size distribution of supra-operonic clusters (SOCs), groups of co-occurring and co-functioning genes that extend beyond operons. Thus, we propose that SOCs form a basic unit of horizontal gene transfer.

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“…Horizontal gene transfer plays an important role in the rapid evolution of bacterial species (Porwollik and McClelland 2003;Soucy et al 2015;Touchon and Rocha 2016). Newly acquired genes have to be integrated not only into their new host physically, but also from a regulatory perspective (Dorman 2007;Higashi et al 2016).…”

Section: Dna Supercoiling Bacterial Evolution and Pathogenesismentioning

confidence: 99%

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Dorman

2016

Biophys Rev

108

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Although it has become routine to consider DNA in terms of its role as a carrier of genetic information, it is also an important contributor to the control of gene expression. This regulatory principle arises from its structural properties. DNA is maintained in an underwound state in most bacterial cells and this has important implications both for DNA storage in the nucleoid and for the expression of genetic information. Underwinding of the DNA through reduction in its linking number potentially imparts energy to the duplex that is available to drive DNA transactions, such as transcription, replication and recombination. The topological state of DNA also influences its affinity for some DNA binding proteins, especially in DNA sequences that have a high A + T base content. The underwinding of DNA by the ATP-dependent topoisomerase DNA gyrase creates a continuum between metabolic flux, DNA topology and gene expression that underpins the global response of the genome to changes in the intracellular and external environments. These connections describe a fundamental and generalised mechanism affecting global gene expression that underlies the specific control of transcription operating through conventional transcription factors. This mechanism also provides a basal level of control for genes acquired by horizontal DNA transfer, assisting microbial evolution, including the evolution of pathogenic bacteria.

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Coevolution of the Organization and Structure of Prokaryotic Genomes

Cited by 59 publications

References 182 publications

Horizontal gene flow into Geobacillus is constrained by the chromosomal organization of growth and sporulation

Horizontal gene flow into Geobacillus is constrained by the chromosomal organization of growth and sporulation

Supra-operonic clusters of functionally related genes (SOCs) are a source of horizontal gene co-transfers

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

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