Recombination in bdelloid rotifer genomes: asexuality, transfer and stress

Bdelloid rotifers constitute a class of microscopic animals living in freshwater habitats worldwide. Several strange features of bdelloids have drawn attention: their ability to tolerate desiccation and other stresses, a lack of reported males across the clade despite centuries of study, and unusually high numbers of horizontally acquired, non-metazoan genes. Genome sequencing is transforming our understanding of their lifestyle and its consequences, while in turn providing wider insights about recombination and genome organisation in animals. Many questions remain, not least how to reconcile apparent genomic signatures of sex with the continued absence of reported males, why bdelloids have so many horizontally acquired genes, and how their remarkable ability to survive stress interacts with recombination and other genomic processes

Comparative genomics of bdelloid rotifers: Insights from desiccating and nondesiccating species.

Bdelloid rotifers are a class of microscopic invertebrates that have existed for millions of years apparently without sex or meiosis. They inhabit a variety of temporary and permanent freshwater habitats globally, and many species are remarkably tolerant of desiccation. Bdelloids offer an opportunity to better understand the evolution of sex and recombination, but previous work has emphasised desiccation as the cause of several unusual genomic features in this group. Here, we present high-quality whole-genome sequences of 3 bdelloid species: Rotaria macrura and R. magnacalcarata, which are both desiccation intolerant, and Adineta ricciae, which is desiccation tolerant. In combination with the published assembly of A. vaga, which is also desiccation tolerant, we apply a comparative genomics approach to evaluate the potential effects of desiccation tolerance and asexuality on genome evolution in bdelloids. We find that ancestral tetraploidy is conserved among all 4 bdelloid species, but homologous divergence in obligately aquatic Rotaria genomes is unexpectedly low. This finding is contrary to current models regarding the role of desiccation in shaping bdelloid genomes. In addition, we find that homologous regions in A. ricciae are largely collinear and do not form palindromic repeats as observed in the published A. vaga assembly. Consequently, several features interpreted as genomic evidence for long-term ameiotic evolution are not general to all bdelloid species, even within the same genus. Finally, we substantiate previous findings of high levels of horizontally transferred nonmetazoan genes in both desiccating and nondesiccating bdelloid species and show that this unusual feature is not shared by other animal phyla, even those with desiccation-tolerant representatives. These comparisons call into question the proposed role of desiccation in mediating horizontal genetic transfer

A high-coverage draft genome of the mycalesine butterfly <i>Bicyclus anynana</i>

The mycalesine butterfly Bicyclus anynana, the "Squinting bush brown," is a model organism in the study of lepidopteran ecology, development, and evolution. Here, we present a draft genome sequence for B. anynana to serve as a genomics resource for current and future studies of this important model species. Seven libraries with insert sizes ranging from 350 bp to 20 kb were constructed using DNA from an inbred female and sequenced using both Illumina and PacBio technology; 128 Gb of raw Illumina data was filtered to 124 Gb and assembled to a final size of 475 Mb (∼×260 assembly coverage). Contigs were scaffolded using mate-pair, transcriptome, and PacBio data into 10 800 sequences with an N50 of 638 kb (longest scaffold 5 Mb). The genome is comprised of 26% repetitive elements and encodes a total of 22 642 predicted protein-coding genes. Recovery of a BUSCO set of core metazoan genes was almost complete (98%). Overall, these metrics compare well with other recently published lepidopteran genomes. We report a high-quality draft genome sequence for Bicyclus anynana. The genome assembly and annotated gene models are available at LepBase (http://ensembl.lepbase.org/index.html)

The Extent of Genome Flux and Its Role in the Differentiation of Bacterial Lineages

Horizontal gene transfer (HGT) and gene loss are key processes in bacterial evolution. However, the role of gene gain and loss in the emergence and maintenance of ecologically differentiated bacterial populations remains an open question. Here, we use whole-genome sequence data to quantify gene gain and loss for 27 lineages of the plant-associated bacterium Pseudomonas syringae. We apply an extensive error-control procedure that accounts for errors in draft genome data and greatly improves the accuracy of patterns of gene occurrence among these genomes. We demonstrate a history of extensive genome fluctuation for this species and show that individual lineages could have acquired thousands of genes in the same period in which a 1% amino acid divergence accrues in the core genome. Elucidating the dynamics of genome fluctuation reveals the rapid turnover of gained genes, such that the majority of recently gained genes are quickly lost. Despite high observed rates of fluctuation, a phylogeny inferred from patterns of gene occurrence is similar to a phylogeny based on amino acid replacements within the core genome. Furthermore, the core genome phylogeny suggests that P. syringae should be considered a number of distinct species, with levels of divergence at least equivalent to those between recognized bacterial species. Gained genes are transferred from a variety of sources, reflecting the depth and diversity of the potential gene pool available via HGT. Overall, our results provide further insights into the evolutionary dynamics of genome fluctuation and implicate HGT as a major factor contributing to the diversification of P. syringae lineages

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Ancestral polymorphisms in Drosophila pseudoobscura and Drosophila miranda

Ancestral polymorphisms are defined as variants that arose by mutation prior to the speciation event that generated the species in which they segregate. Their presence may complicate the interpretation of molecular data and lead to incorrect phylogenetic inferences. They may also be used to identify regions of the genome that are under balancing selection. It is thus important to take into account the contribution of ancestral polymorphisms to variability within species and divergence between species. Here, we extend and improve a method for estimation of the proportion of ancestral polymorphisms within a species, and apply it to a dataset of 33 X-linked and 34 autosomal protein-coding genes for which sequence polymorphism data are available in both Drosophila pseudoobscura and Drosophila miranda, using Drosophila affinis as an outgroup. We show that a substantial proportion of both X-linked and autosomal synonymous variants in these two species are ancestral, and that a small number of additional genes with unusually high sequence diversity seem to have an excess of ancestral polymorphisms, suggestive of balancing selection

Historical genomics reveals the evolutionary mechanisms behind multiple outbreaks of the host-specific coffee wilt pathogen Fusarium xylarioides

Background: Nearly 50% of crop yields are lost to pests and disease, with plants and pathogens locked in an amplified co-evolutionary process of disease outbreaks. Coffee wilt disease, caused by Fusarium xylarioides, decimated coffee production in west and central Africa following its initial outbreak in the 1920s. After successful management, it later re-emerged and by the 2000s comprised two separate epidemics on arabica coffee in Ethiopia and robusta coffee in east and central Africa. Results: Here, we use genome sequencing of six historical culture collection strains spanning 52 years to identify the evolutionary processes behind these repeated outbreaks. Phylogenomic reconstruction using 13,782 single copy orthologs shows that the robusta population arose from the initial outbreak, whilst the arabica population is a divergent sister clade to the other strains. A screen for putative effector genes involved in pathogenesis shows that the populations have diverged in gene content and sequence mainly by vertical processes within lineages. However, 15 putative effector genes show evidence of horizontal acquisition, with close homology to genes from F. oxysporum. Most occupy small regions of homology within wider scaffolds, whereas a cluster of four genes occupy a 20Kb scaffold with strong homology to a region on a mobile pathogenicity chromosome in F. oxysporum that houses known effector genes. Lacking a match to the whole mobile chromosome, we nonetheless found close associations with DNA transposons, especially the miniature impala type previously proposed to facilitate horizontal transfer of pathogenicity genes in F. oxysporum. These findings support a working hypothesis that the arabica and robusta populations partly acquired distinct effector genes via transposition-mediated horizontal transfer from F. oxysporum, which shares coffee as a host and lives on other plants intercropped with coffee. Conclusion: Our results show how historical genomics can help reveal mechanisms that allow fungal pathogens to keep pace with our efforts to resist them. Our list of putative effector genes identifies possible future targets for fungal control. In turn, knowledge of horizontal transfer mechanisms and putative donor taxa might help to design future intercropping strategies that minimize the risk of transfer of effector genes between closely-related Fusarium taxa

Comparative genomics of Alexander Fleming’s original Penicillium isolate (IMI 15378) reveals sequence divergence of penicillin synthesis genes

Antibiotics were derived originally from wild organisms and therefore understanding how these compounds evolve among different lineages might help with the design of new antimicrobial drugs. We report the draft genome sequence of Alexander Fleming’s original fungal isolate behind the discovery of penicillin, now classified as Penicillium rubens Biourge (1923) (IMI 15378). We compare the structure of the genome and genes involved in penicillin synthesis with those in two ‘high producing’ industrial strains of P. rubens and the closely related species P. nalgiovense. The main effector genes for producing penicillin G (pcbAB, pcbC and penDE) show amino acid divergence between the Fleming strain and both industrial strains, whereas a suite of regulatory genes are conserved. Homologs of penicillin N effector genes cefD1 and cefD2 were also found and the latter displayed amino acid divergence between the Fleming strain and industrial strains. The draft assemblies contain several partial duplications of penicillin-pathway genes in all three P. rubens strains, to differing degrees, which we hypothesise might be involved in regulation of the pathway. The two industrial strains are identical in sequence across all effector and regulatory genes but differ in duplication of the pcbAB–pcbC–penDE complex and partial duplication of fragments of regulatory genes. We conclude that evolution in the wild encompassed both sequence changes of the effector genes and gene duplication, whereas human-mediated changes through mutagenesis and artificial selection led to duplication of the penicillin pathway genes.ISSN:2045-232

Author response: Evolutionary dynamics of transposable elements in bdelloid rotifers

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Evolutionary dynamics of transposable elements in bdelloid rotifers

Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates in which males are thus far unknown. Contrary to expectations, we find a variety of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms. Instead, we find that that TE content evolves relatively slowly in bdelloids and that gene families involved in RNAi-mediated TE suppression have undergone significant expansion, which might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.publishe