Why Genes Evolve Faster on Secondary Chromosomes in Bacteria

Cooper, Vaughn S.; Vohr, Samuel H.; Wrocklage, Sarah C.; Hatcher, Philip J.

doi:10.1371/journal.pcbi.1000732

Cited by 100 publications

(151 citation statements)

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“…Our data demonstrate that base-substitution mutation rates vary significantly among chromosomes, but not in the direction predicted by comparative studies on sequence divergence (Mira and Ochman 2002;Cooper et al 2010;Lang and Murray 2011;Agier and Fischer 2012;. Specifically, we find that base-substitution mutation rates are highest on the primary chromosome ( Figure 3, A and B), where evolutionary rates are lowest.…”

Section: Discussioncontrasting

confidence: 44%

“…= 2, P = 0.034) ( Figure 3A). Specifically, base-substitution mutation rates are highest on Chr1, and lowest on Chr2, which is the opposite of observed evolutionary rates on these chromosomes (see Figure S5) (Cooper et al 2010). In addition, a second chi-squared test was performed to test whether the observed base-substitution mutation rates differed from the conditional mutation rates expected on each chromosome given their respective nucleotide contents, which are similar (%GC: Chr1, 66.8%; Chr2, 66.9%; and Chr3, 67.3%).…”

Section: Nonuniform Chromosomal Distribution Of Mutationsmentioning

confidence: 72%

“…Chromosome 1 (Chr1) is the largest chromosome (both in size and in gene count), with more essential and highly expressed genes than either chromosome 2 (Chr2) or 3 (Chr3) (see Figure S5). Expression and number of essential genes are second highest on Chr2 and lowest on Chr3 (Cooper et al 2010;. In contrast, average nonsynonymous and synonymous variation among orthologs shared by multiple strains of B. cenocepacia, as well as fixed variation among Burkholderia species (dN and dS), are highest on Chr3 and lowest on Chr1 (see Figure S5) (Cooper et al 2010;.…”

Section: Nonuniform Chromosomal Distribution Of Mutationsmentioning

confidence: 99%

“…Studies in Vibrio cholerae have suggested that in bacteria with multiple chromosomes, smaller secondary chromosomes delay their replication until there remains approximately the same number of bases to be replicated on larger chromosomes Cooper et al 2010). This ensures synchrony of replication termination between chromosomes of different sizes, despite the fact that their replication proceeds at the same rate.…”

Section: Nonuniform Chromosomal Distribution Of Mutationsmentioning

confidence: 99%

“…In addition, B. cenocepacia HI2424 contains a 0.164-Mb plasmid, which contains 159 genes and lower %GC content than the core genome (62.0%). Although the %GC content is consistent across the three core chromosomes, the proportion of coding DNA declines from Chr1 to Chr3, while the synonymous and nonsynonymous substitution rates increase from Chr1 to Chr3 (Cooper et al 2010;. Whether this variation in evolutionary rate is driven by variation in nonadaptive processes like mutation bias or variation in the relative strength of purifying selection remains a largely unanswered question in the evolution of bacteria with multiple chromosomes.…”

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The Rate and Molecular Spectrum of Spontaneous Mutations in the GC-Rich Multichromosome Genome of Burkholderia cenocepacia

et al. 2015

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Spontaneous mutations are ultimately essential for evolutionary change and are also the root cause of many diseases. However, until recently, both biological and technical barriers have prevented detailed analyses of mutation profiles, constraining our understanding of the mutation process to a few model organisms and leaving major gaps in our understanding of the role of genome content and structure on mutation. Here, we present a genome-wide view of the molecular mutation spectrum in Burkholderia cenocepacia, a clinically relevant pathogen with high %GC content and multiple chromosomes. We find that B. cenocepacia has low genome-wide mutation rates with insertion-deletion mutations biased toward deletions, consistent with the idea that deletion pressure reduces prokaryotic genome sizes. Unlike prior studies of other organisms, mutations in B. cenocepacia are not AT biased, which suggests that at least some genomes with high %GC content experience unusual base-substitution mutation pressure. Importantly, we also observe variation in both the rates and spectra of mutations among chromosomes and elevated G:C . T:A transversions in late-replicating regions. Thus, although some patterns of mutation appear to be highly conserved across cellular life, others vary between species and even between chromosomes of the same species, potentially influencing the evolution of nucleotide composition and genome architecture.KEYWORDS mutation rate; genome evolution; replication timing; mutation spectra A S the ultimate source of genetic variation, mutation is implicit in every aspect of genetics and evolution. However, as a result of the genetic burden imposed by deleterious mutations, remarkably low mutation rates have evolved across all of life, making detection of these rare events technologically challenging and accurate measures of mutation rates and spectra exceedingly difficult (Kibota and Lynch 1996;Lynch and Walsh 1998;Sniegowski et al. 2000;Lynch 2011;Fijalkowska et al. 2012;Zhu et al. 2014). Until recently, most estimates of mutational properties have been derived indirectly using comparative genomics at putatively neutral sites (Graur and Li 2000;Wielgoss et al. 2011) or by extrapolation from small reporter-construct studies (Drake 1991). Both of these methods are subject to potentially significant biases, as many putatively neutral sites are subject to selection and mutation rates can vary substantially among different genomic regions (Lynch 2007).To avoid the potential biases of these earlier methods, pairing classic mutation accumulation (MA) with wholegenome sequencing (WGS) has become the preferred method for obtaining direct measures of mutation rates and spectra (Lynch et al. 2008;Denver et al. 2009;Ossowski et al. 2010;Lee et al. 2012; Sung et al. 2012a,b;Heilbron et al. 2014). Using this strategy, a single clonal ancestor is used to initiate several replicate lineages that are subsequently passaged through repeated single-cell bottlenecks for several thousand generations. The complete genomes of ea...

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Section: Discussioncontrasting

confidence: 44%

Section: Nonuniform Chromosomal Distribution Of Mutationsmentioning

confidence: 72%

Section: Nonuniform Chromosomal Distribution Of Mutationsmentioning

confidence: 99%

Section: Nonuniform Chromosomal Distribution Of Mutationsmentioning

confidence: 99%

mentioning

confidence: 99%

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The Rate and Molecular Spectrum of Spontaneous Mutations in the GC-Rich Multichromosome Genome of Burkholderia cenocepacia

et al. 2015

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Burkholderia

Vandamme¹,

Eberl²

2018

Bergey's Manual of Systematics of Archaea and Bacteria

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Burk.hol.de'ri.a. N.L. fem. n. Burkholderia named after W. H. Burkholder, American bacteriologist who discovered the etiological agent of onion rot. Proteobacteria / Betaproteobacteria / Burkholderiales / Burkholderiaceae / Burkholderia The genus Burkholderia now groups more than 100 species with extraordinary metabolic capacities, and which occupy a bewildering array of ecological niches. The sources from which Burkholderia species have been isolated are manifold, but the accumulated evidence suggests that soil, where Burkholderia can be associated with a wide range of plants and fungi, is its natural habitat. The genus comprises two class‐3 pathogens, Burkholderia mallei and Burkholderia pseudomallei , but a growing number of Burkholderia species has been reported as opportunistic pathogens in humans. Burkholderia bacteria appear to have a predilection for the respiratory tract as life‐threatening lung infections occur in individuals with cystic fibrosis or chronic granulomatous disease, and in patients requiring mechanical ventilation. Burkholderia bacteria have rightfully been referred to as both friend and foe to humans. While the first Burkholderia species were primarily known as plant, human, and animal pathogens, subsequent studies revealed their biotechnological potential for plant growth promotion, biocontrol of various plant pests, and bioremediation. Because of this wide interest, an unusual number of whole‐genome sequences has become available, yet generally failed to reveal the difference between good or bad, or alternatively, biotechnologically safe or unsafe, species or strains. The phylogenetic diversity within this genus was recently used as an argument to reclassify the large majority of Burkholderia species into Burkholderia sensu stricto and the novel genera Caballeronia, Paraburkholderia , and Robbsia . Except for the latter, each of genera consists of environmental species of which a growing number is reported to cause infections in humans. DNA G + C content (mol%) : 64–69. Type species : Burkholderia cepacia (Palleroni and Holmes 1981) Yabuuchi, Kosako, Oyaizu, Yano, Hotta, Hashimoto, Ezaki and Arakawa 1993, 398 VP (Effective publication: Yabuuchi, Kosako, Oyaizu, Yano, Hotta, Hashimoto, Ezaki and Arakawa 1992, 1271) ( Pseudomonas cepacia Palleroni and Holmes 1981, 479).

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Plasmids as Secondary Chromosomes

Mergeay¹

2018

Molecular Life Sciences

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Why Genes Evolve Faster on Secondary Chromosomes in Bacteria

Cited by 100 publications

References 50 publications

The Rate and Molecular Spectrum of Spontaneous Mutations in the GC-Rich Multichromosome Genome of Burkholderia cenocepacia

The Rate and Molecular Spectrum of Spontaneous Mutations in the GC-Rich Multichromosome Genome of Burkholderia cenocepacia

Burkholderia

Plasmids as Secondary Chromosomes

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