Dataset Information

Systematic identification of gene-altering programmed inversions across the bacterial domain.

ABSTRACT: Programmed chromosomal inversions allow bacteria to generate intra-population genotypic and functional heterogeneity, a bet-hedging strategy important in changing environments. Some programmed inversions modify coding sequences, producing different alleles in several gene families, most notably in specificity-determining genes such as Type I restriction-modification systems, where systematic searches revealed cross phylum abundance. Yet, a broad, gene-independent, systematic search for gene-altering programmed inversions has been absent, and little is known about their genomic sequence attributes and prevalence across gene families. Here, identifying intra-species variation in genomes of over 35 000 species, we develop a predictive model of gene-altering inversions, revealing key attributes of their genomic sequence attributes, including gene-pseudogene size asymmetry and orientation bias. The model predicted over 11,000 gene-altering loci covering known targeted gene families, as well as novel targeted families including Type II restriction-modification systems, a protein of unknown function, and a fusion-protein containing conjugative-pilus and phage tail domains. Publicly available long-read sequencing datasets validated representatives of these newly predicted inversion-targeted gene families, confirming intra-population genetic heterogeneity. Together, these results reveal gene-altering programmed inversions as a key strategy adopted across the bacterial domain, and highlight programmed inversions that modify Type II restriction-modification systems as a possible new mechanism for maintaining intra-population heterogeneity.

SUBMITTER: Milman O

PROVIDER: S-EPMC9881135 | biostudies-literature | 2023 Jan

REPOSITORIES: biostudies-literature

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Systematic identification of gene-altering programmed inversions across the bacterial domain.

Milman Oren O Yelin Idan I Kishony Roy R

Nucleic acids research 20230101 2

Programmed chromosomal inversions allow bacteria to generate intra-population genotypic and functional heterogeneity, a bet-hedging strategy important in changing environments. Some programmed inversions modify coding sequences, producing different alleles in several gene families, most notably in specificity-determining genes such as Type I restriction-modification systems, where systematic searches revealed cross phylum abundance. Yet, a broad, gene-independent, systematic search for gene-alte ...[more]

PMID: 36617974

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Project description:Polymorphic inversions are a source of genetic variability with a direct impact on recombination frequencies. Given the difficulty of their experimental study, computational methods have been developed to infer their existence in a large number of individuals using genome-wide data of nucleotide variation. Methods based on haplotype tagging of known inversions attempt to classify individuals as having a normal or inverted allele. Other methods that measure differences between linkage disequilibrium attempt to identify regions with inversions but unable to classify subjects accurately, an essential requirement for association studies.We present a novel method to both identify polymorphic inversions from genome-wide genotype data and classify individuals as containing a normal or inverted allele. Our method, a generalization of a published method for haplotype data 1, utilizes linkage between groups of SNPs to partition a set of individuals into normal and inverted subpopulations. We employ a sliding window scan to identify regions likely to have an inversion, and accumulation of evidence from neighboring SNPs is used to accurately determine the inversion status of each subject. Further, our approach detects inversions directly from genotype data, thus increasing its usability to current genome-wide association studies (GWAS).We demonstrate the accuracy of our method to detect inversions and classify individuals on principled-simulated genotypes, produced by the evolution of an inversion event within a coalescent model 2. We applied our method to real genotype data from HapMap Phase III to characterize the inversion status of two known inversions within the regions 17q21 and 8p23 across 1184 individuals. Finally, we scan the full genomes of the European Origin (CEU) and Yoruba (YRI) HapMap samples. We find population-based evidence for 9 out of 15 well-established autosomic inversions, and for 52 regions previously predicted by independent experimental methods in ten (9+1) individuals 34. We provide efficient implementations of both genotype and haplotype methods as a unified R package inveRsion.

Dataset Information

Systematic identification of gene-altering programmed inversions across the bacterial domain.

Publications

Systematic identification of gene-altering programmed inversions across the bacterial domain.

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