Large-Scale Genomic Analysis Suggests a Neutral Punctuated Dynamics of Transposable Elements in Bacterial Genomes

Iranzo, Jaime; Gómez, Manuel J.; Saro, Francisco J. López de; Manrubia, Susanna C.

doi:10.1371/journal.pcbi.1003680

Cited by 35 publications

(45 citation statements)

References 59 publications

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“…A possible solution comes from our observation that the HGT to loss ratio (where the HGT rate is measured per genome and the loss rate is measured per gene) grows with the genome size. Such behavior, which had been already noted for transposons (23) and agrees with the recently derived genome-average scaling law (14), is likely to result, at least in part, from larger genomes providing more nonessential regions where a parasite can integrate without incurring major costs to the cell. Alternatively or additionally, the observed dependence could emerge if duplication and loss rates per gene decreased with genome size, whereas the HGT rate remains constant.…”

Section: Discussionsupporting

confidence: 84%

“…Multiple variants of the duplication-transfer-loss model and related multitype branching processes have been widely used to study the evolution of gene copy numbers (24,25,28,49), especially in the context of transposons and other genetic parasites (22,23,26,27,50). To make the models tractable, most studies make simplifying assumptions, such as stationary state, absence of duplication, or lack of selection, and obtain the model parameters from the copy number distributions observed in large genomic datasets, relying on the assumption that model parameters are homogeneous across taxa.…”

Section: Discussionmentioning

confidence: 99%

“…For the purpose of evolutionary analyses, a meaningful proxy for such an average can be obtained by inferring selection coefficients directly from the gene family abundances observed in large collections of genomes. The main difficulty in this case is disentangling the effects of selection from the effects of intrinsic loss bias, which normally requires a priori knowledge of the effective population size or the gene gain and loss rates (14,22,23).…”

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confidence: 99%

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Disentangling the effects of selection and loss bias on gene dynamics

Iranzo

Cuesta

Manrubia

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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We combine mathematical modeling of genome evolution with comparative analysis of prokaryotic genomes to estimate the relative contributions of selection and intrinsic loss bias to the evolution of different functional classes of genes and mobile genetic elements (MGE). An exact solution for the dynamics of gene family size was obtained under a linear duplication-transfer-loss model with selection. With the exception of genes involved in information processing, particularly translation, which are maintained by strong selection, the average selection coefficient for most nonparasitic genes is low albeit positive, compatible with observed positive correlation between genome size and effective population size. Free-living microbes evolve under stronger selection for gene retention than parasites. Different classes of MGE show a broad range of fitness effects, from the nearly neutral transposons to prophages, which are actively eliminated by selection. Genes involved in antiparasite defense, on average, incur a fitness cost to the host that is at least as high as the cost of plasmids. This cost is probably due to the adverse effects of autoimmunity and curtailment of horizontal gene transfer caused by the defense systems and selfish behavior of some of these systems, such as toxin-antitoxin and restriction modification modules. Transposons follow a biphasic dynamics, with bursts of gene proliferation followed by decay in the copy number that is quantitatively captured by the model. The horizontal gene transfer to loss ratio, but not duplication to loss ratio, correlates with genome size, potentially explaining increased abundance of neutral and costly elements in larger genomes.

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Section: Discussionsupporting

confidence: 84%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Disentangling the effects of selection and loss bias on gene dynamics

Iranzo

Cuesta

Manrubia

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…These observations are in accordance with the proposed neutral punctuated model for IS elements proliferation (Iranzo et al, 2014). This model predicts instability of IS copy number following a change in the environment, such as that following the establishment of a host-specific lifestyle.…”

Section: Reductive Genome Evolution In Leaf Nodule Symbiontssupporting

confidence: 88%

Evidence of horizontal gene transfer between obligate leaf nodule symbionts

Pinto‐Carbó¹,

Sieber²,

Dessein³

et al. 2016

The ISME Journal

105

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Bacteria of the genus Burkholderia establish an obligate symbiosis with plant species of the Rubiaceae and Primulaceae families. The bacteria, housed within the leaves, are transmitted hereditarily and have not yet been cultured. We have sequenced and compared the genomes of eight bacterial leaf nodule symbionts of the Rubiaceae plant family. All of the genomes exhibit features consistent with genome erosion. Genes potentially involved in the biosynthesis of kirkamide, an insecticidal C7N aminocyclitol, are conserved in most Rubiaceae symbionts. However, some have partially lost the kirkamide pathway due to genome erosion and are unable to synthesize the compound. Kirkamide synthesis is therefore not responsible for the obligate nature of the symbiosis. More importantly, we find evidence of intra-clade horizontal gene transfer (HGT) events affecting genes of the secondary metabolism. This indicates that substantial gene flow can occur at the early stages following host restriction in leaf nodule symbioses. We propose that host-switching events and plasmid conjugative transfers could have promoted these HGTs. This genomic analysis of leaf nodule symbionts gives, for the first time, new insights in the genome evolution of obligate symbionts in their early stages of the association with plants.

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“…In recent years, the availability of large datasets for comparative genomics has opened new pathways for the study of genetic parasites. Concomitantly, some existing models have been revisited to investigate the dynamics of insertion sequences (a class of transposons) in bacteria, concluding that the observed abundances are compatible with a scenario of low fitness cost [42,43].…”

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confidence: 99%

How genetic parasites persist despite the purge of natural selection

Iranzo

Koonin

2018

EPL

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-Genetic parasites, such as transposons, plasmids and viruses, are ubiquitous in cellular life forms. Although the selfish nature of these genetic elements is undeniable, the actual cost that they impose on their host and the mechanisms by which they counteract natural selection remain unclear. We combined mathematical models and comparative genomics to disentangle the roles of selection, horizontal gene transfer, gene duplication and gene loss in the spread and persistence of genetic parasites. By quantifying the mean contribution of transposons, conjugative plasmids, prophages and toxin-antitoxin modules to the fitness of microbial hosts, we provide evidence that these genetic elements are deleterious at evolutionary timescales. Moreover, the transfer rates experienced by selfish genetic elements exceed the minimum rates required for their long-term survival, which fully characterizes these elements as parasites.

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Large-Scale Genomic Analysis Suggests a Neutral Punctuated Dynamics of Transposable Elements in Bacterial Genomes

Cited by 35 publications

References 59 publications

Disentangling the effects of selection and loss bias on gene dynamics

Disentangling the effects of selection and loss bias on gene dynamics

Evidence of horizontal gene transfer between obligate leaf nodule symbionts

How genetic parasites persist despite the purge of natural selection

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