Measuring the impact of gene prediction on gene loss estimates in Eukaryotes by quantifying falsely inferred absences

Deutekom, Eva S.; Vosseberg, Julian; Dam, Teunis J. P. van; Snel, Berend

doi:10.1371/journal.pcbi.1007301

Cited by 48 publications

(54 citation statements)

References 38 publications

(62 reference statements)

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“…In comparative genomics studies, misleading conclusions can arise when the variable of interest (e.g., the evolution of herbivory) is biologically confounded with a causal variable (e.g., demographic events) (20) , or with a bioinformatic approach that lacks sensitivity or imparts lineage-specific biases (66) . We considered three strong sources of potential confounding in S. flava -shifts in demography (e.g., population size); artifactually missing, collapsed, or duplicated regions of the genome assembly; and incomplete gene annotations.…”

Section: Robustness Of Findings To Biological and Bioinformatic Confomentioning

confidence: 99%

Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

Preprint

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SIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly ( Drosophila melanogaste r), the "wasabi fly" ( Scaptomyza flava ), that evolved to consume mustard plants including Arabidopsis thaliana . The yeast-to-mustard dietary transition remodeled the fly's gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals. Gloss et al. 2019 1ABSTRACT One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana ) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila . We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains ("blooms") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase ( Gst ) and cytochrome P450 ( Cyp450 ) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1 ) and Gst (N=5 for GstE5-8 ) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro . One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis , helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.

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Section: Robustness Of Findings To Biological and Bioinformatic Confomentioning

confidence: 99%

Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

Preprint

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“…4). In the wake of symbiogenic mergers, which are very rare in evolution, gene loss sets in, whereby gene loss is very common in eukaryote genome evolution, one of its main underlying themes [41,45].…”

Section: Parasites With Their Reduced Genomes Such As Giardia Lamblmentioning

confidence: 99%

Bacterial genes outnumber archaeal genes in eukaryotic genomes

Bruckner

Martin

2019

Preprint

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AbstractThe origin of eukaryotes is one of evolution’s most important transitions, yet it is still poorly understood. Evidence for how it occurred should be preserved in eukaryotic genomes. Based on phylogenetic trees from ribosomal RNA and ribosomal proteins, eukaryotes are typically depicted as branching together with or within archaea. This ribosomal affiliation is widely interpreted as evidence for an archaeal origin of eukaryotes. However, the extent to which the archaeal ancestry of genes for the cytosolic ribosomes of eukaryotic cells is representative for the rest of the eukaryotic genome is unknown. Here we have clustered 19,050,992 protein sequences from 5,443 bacteria and 212 archaea with 3,420,731 protein sequences from 150 eukaryotes spanning six eukaryotic supergroups to identify genes that link eukaryotes exclusively to bacteria and archaea respectively. By downsampling the bacterial sample we obtain estimates for the bacterial and archaeal proportions of genes among 150 eukaryotic genomes. Eukaryotic genomes possess a bacterial majority of genes. On average, eukaryotic genes are 56% bacterial in origin. The majority drops to 53% in eukaryotes that never possessed plastids, and increases to 61% in photosynthetic eukaryotic lineages, where the cyanobacterial ancestor of plastids contributed additional genes to the eukaryotic genome, reaching 67% in higher plants. Intracellular parasites, which undergo reductive evolution in adaptation to the nutrient rich environment of the cells that they infect, relinquish bacterial genes for metabolic processes. In the current sample, this process of adaptive gene loss is most pronounced in the human parasite Encephalitozoon intestinalis with 86% archaeal and 14% bacterial derived genes. The most bacterial eukaryote genome sampled is rice, with 67% bacterial and 33% archaeal genes. The functional dichotomy, initially described for yeast, of archaeal genes being involved in genetic information processing and bacterial genes being involved in metabolic processes is conserved across all eukaryotic supergroups.

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“…Taking the absence of genes in annotated gene sets at face value can, therefore, lead to wrong evolutionary inferences (Deutekom, et al 2019). However, for 33 LCALec genes we could find, to this point, no indication of an experimental artefact, and they appear genuinely absent from the U. pustulata genome (supplementary table S8, Supplementary Material online).…”

Section: Lineage Specific Absence Of Evolutionarily Old Genes In U Pmentioning

confidence: 99%

What is in a lichen? A metagenomic approach to reconstruct the holo-genome of Umbilicaria pustulata

Bicker

et al. 2019

Preprint

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Lichens are valuable models in symbiosis research and promising sources of biosynthetic genes for biotechnological applications. Most lichenized fungi grow slowly, resist aposymbiotic cultivation, and are generally poor candidates for experimentation. Obtaining contiguous, high quality genomes for such symbiotic communities is technically challenging. Here we present the first assembly of a lichen holo-genome from metagenomic whole genome shotgun data comprising both PacBio long reads and Illumina short reads. The nuclear genomes of the two primary components of the lichen symbiosisthe fungus Umbilicaria pustulata (33 Mbp) and the green alga Trebouxia sp. (53 Mbp)were assembled at contiguities comparable to single-species assemblies. The analysis of the read coverage pattern revealed a relative cellular abundance of approximately 20:1 (fungus:alga). Gap-free, circular sequences for all organellar genomes were obtained. The community of lichen-associated bacteria is dominated by Acidobacteriaceae, and the two largest bacterial contigs belong to the genus Acidobacterium. Gene set analyses showed no evidence of horizontal gene transfer from algae or bacteria into the fungal genome. Our data suggest a lineagespecific loss of a putative gibberellin-20-oxidase in the fungus, a gene fusion in the fungal mitochondrion, and a relocation of an algal chloroplast gene to the algal nucleus.Major technical obstacles during reconstruction of the holo-genome were coverage differences among individual genomes surpassing three orders of magnitude.Moreover, we show that G/C-rich inverted repeats paired with non-random sequencing error in PacBio data can result in missing gene predictions. This likely poses a general problem for genome assemblies based on long reads.

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Measuring the impact of gene prediction on gene loss estimates in Eukaryotes by quantifying falsely inferred absences

Cited by 48 publications

References 38 publications

Evolution of herbivory remodels aDrosophilagenome

Evolution of herbivory remodels aDrosophilagenome

Bacterial genes outnumber archaeal genes in eukaryotic genomes

What is in a lichen? A metagenomic approach to reconstruct the holo-genome of Umbilicaria pustulata

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