The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming
TL;DR: These first analyses of the A. echinatior genome indicate that considerable genetic changes are likely to have accompanied the transition from hunter-gathering to agricultural food production 50 million years ago, and the Transition from single to multiple queen mating 10 million years years ago.
Abstract: We present a high-quality (>100 3depth) Illumina genome sequence of the leaf-cutting ant Acromyrmex echinatior, a model speciesforsymbiosisandreproductiveconflictstudies. Wecompare thisgenomewiththreepreviouslysequenced genomes of ants from different subfamilies and focus our analyses on aspects of the genome likely to be associated with known evolutionary changes. The first is the specialized fungal diet of A. echinatior, where we find gene loss in the ant’s arginine synthesis pathway, loss of detoxification genes, and expansion of a group of peptidase proteins. One of these is a unique ant-derived contribution to the fecal fluid, which otherwise consists of ‘‘garden manuring’’ fungal enzymes that are unaffected by antdigestion.Thesecond is multiplemating ofqueens andejaculatecompetition,which maybe associatedwith a greatly expanded nardilysin-like peptidase gene family. The third is sex determination, where we could identify only a single homolog of the feminizer gene. As other ants and the honeybee have duplications of this gene, we hypothesize that this may partly explain the frequent production of diploid male larvae in A. echinatior. The fourth is the evolution of eusociality, where we find a highly conserved ant-specific profile of neuropeptide genes that may be related to caste determination. These first analyses of the A. echinatior genome indicate that considerable genetic changes are likely to have accompaniedthetransitionfromhunter-gathering toagriculturalfoodproduction50millionyearsago,andthetransition from single to multiple queen mating 10 million years ago. [Supplemental material is available for this article.]
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01 Jan 2000
3,536 citations
Commonwealth Scientific and Industrial Research Organisation1, Rutgers University2, Heidelberg Institute for Theoretical Studies3, University of Jena4, University of Bonn5, Naturhistorisches Museum6, University of Vienna7, University of Tsukuba8, Landcare Research9, Johns Hopkins University10, University of Hamburg11, Ehime University12, Florida Museum of Natural History13, Staatliches Museum für Naturkunde Stuttgart14, National Evolutionary Synthesis Center15, Australian National University16, Macquarie University17, American Museum of Natural History18, University of Memphis19, University of Guadalajara20, Bavarian Academy of Sciences and Humanities21, Natural History Museum22, Karlsruhe Institute of Technology23, California Academy of Sciences24, South China Agricultural University25, North Carolina State University26, Hokkaido University27
TL;DR: The phylogeny of all major insect lineages reveals how and when insects diversified and provides a comprehensive reliable scaffold for future comparative analyses of evolutionary innovations among insects.
Abstract: Insects are the most speciose group of animals, but the phylogenetic relationships of many major lineages remain unresolved. We inferred the phylogeny of insects from 1478 protein-coding genes. Phylogenomic analyses of nucleotide and amino acid sequences, with site-specific nucleotide or domain-specific amino acid substitution models, produced statistically robust and congruent results resolving previously controversial phylogenetic relations hips. We dated the origin of insects to the Early Ordovician [~479 million years ago (Ma)], of insect flight to the Early Devonian (~406 Ma), of major extant lineages to the Mississippian (~345 Ma), and the major diversification of holometabolous insects to the Early Cretaceous. Our phylogenomic study provides a comprehensive reliable scaffold for future comparative analyses of evolutionary innovations among insects.
1,998 citations
TL;DR: An overview of the genome annotation process and the available tools is provided and some best-practice approaches are described.
Abstract: The falling cost of genome sequencing is having a marked impact on the research community with respect to which genomes are sequenced and how and where they are annotated. Genome annotation projects have generally become small-scale affairs that are often carried out by an individual laboratory. Although annotating a eukaryotic genome assembly is now within the reach of non-experts, it remains a challenging task. Here we provide an overview of the genome annotation process and the available tools and describe some best-practice approaches.
604 citations
Staatliches Museum für Naturkunde Stuttgart1, University of Freiburg2, Heidelberg Institute for Theoretical Studies3, University of Bonn4, Australian National University5, National Scientific and Technical Research Council6, University of California, Riverside7, Rutgers University8, Naturhistorisches Museum9, National University of Singapore10, University of Castilla–La Mancha11, University of Würzburg12, University of Copenhagen13, China Agricultural University14, Arizona State University15
TL;DR: The results reveal that the extant sawfly diversity is largely the result of a previously unrecognized major radiation of phytophagous Hymenoptera that did not lead to wood-dwelling and parasitoidism.
549 citations
University of Washington1, University of Missouri2, Baylor College of Medicine3, University of Düsseldorf4, Pompeu Fabra University5, Ghent University6, Johns Hopkins University7, Agricultural Research Service8, University of British Columbia9, University of Houston10, University of Illinois at Urbana–Champaign11, Purdue University12, University of Pittsburgh13, Australian National University14, Martin Luther University of Halle-Wittenberg15, Lawrence Berkeley National Laboratory16, National Institutes of Health17, University of North Carolina at Greensboro18, King Abdullah University of Science and Technology19, Clemson University20, Swiss Institute of Bioinformatics21
TL;DR: Improved honey bee genome assembly with a new gene annotation set and a number of genes similar to that of other insect genomes are reported, contrary to what was suggested in OGSv1.0.
Abstract: The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching finished quality (human, mouse, fly and worm), there is room for improvement of most genome assemblies. The honey bee (Apis mellifera) genome, published in 2006, was noted for its bimodal GC content distribution that affected the quality of the assembly in some regions and for fewer genes in the initial gene set (OGSv1.0) compared to what would be expected based on other sequenced insect genomes. Here, we report an improved honey bee genome assembly (Amel_4.5) with a new gene annotation set (OGSv3.2), and show that the honey bee genome contains a number of genes similar to that of other insect genomes, contrary to what was suggested in OGSv1.0. The new genome assembly is more contiguous and complete and the new gene set includes ~5000 more protein-coding genes, 50% more than previously reported. About 1/6 of the additional genes were due to improvements to the assembly, and the remaining were inferred based on new RNAseq and protein data. Lessons learned from this genome upgrade have important implications for future genome sequencing projects. Furthermore, the improvements significantly enhance genomic resources for the honey bee, a key model for social behavior and essential to global ecology through pollination.
370 citations
Cites background from "The genome of the leaf-cutting ant ..."
...Recently sequenced Hymenoptera genomes (parasitoid w asp and seven ant species), predicted to contain ~17,000-18,500 protein-coding genes [18-24], further support the suspicion that a large number of A....
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...5%, Acromyrmex echinator 27%, Harpegnathos saltator 27%, Solenopsis invicta >23%) and the genome of the parasitoid wasp, Nasonia vitripennis, contains more than three times the amount (>30%) [18-20,22-24]....
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References
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TL;DR: A new criterion for triggering the extension of word hits, combined with a new heuristic for generating gapped alignments, yields a gapped BLAST program that runs at approximately three times the speed of the original.
Abstract: The BLAST programs are widely used tools for searching protein and DNA databases for sequence similarities. For protein comparisons, a variety of definitional, algorithmic and statistical refinements described here permits the execution time of the BLAST programs to be decreased substantially while enhancing their sensitivity to weak similarities. A new criterion for triggering the extension of word hits, combined with a new heuristic for generating gapped alignments, yields a gapped BLAST program that runs at approximately three times the speed of the original. In addition, a method is introduced for automatically combining statistically significant alignments produced by BLAST into a position-specific score matrix, and searching the database using this matrix. The resulting Position-Specific Iterated BLAST (PSIBLAST) program runs at approximately the same speed per iteration as gapped BLAST, but in many cases is much more sensitive to weak but biologically relevant sequence similarities. PSI-BLAST is used to uncover several new and interesting members of the BRCT superfamily.
70,111 citations
"The genome of the leaf-cutting ant ..." refers methods in this paper
...We used BLAST (Altschul et al. 1997) to assign genes to functional categories defined in the Kyoto Encyclopedia of Genes and Genomes (KEGG categories) (Kanehisa and Goto 2000) and examined the annotations to identify metabolic pathways where A. echinatior had an apparent loss-of-function compared…...
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...We then annotated 17,278 protein-coding genes by using GLEAN (Elsik et al. 2007) to integrate de novo gene predictions, tran- scriptome evidence, and BLAST (Altschul et al. 1997) homology information....
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TL;DR: MUSCLE is a new computer program for creating multiple alignments of protein sequences that includes fast distance estimation using kmer counting, progressive alignment using a new profile function the authors call the log-expectation score, and refinement using tree-dependent restricted partitioning.
Abstract: We describe MUSCLE, a new computer program for creating multiple alignments of protein sequences. Elements of the algorithm include fast distance estimation using kmer counting, progressive alignment using a new profile function we call the logexpectation score, and refinement using treedependent restricted partitioning. The speed and accuracy of MUSCLE are compared with T-Coffee, MAFFT and CLUSTALW on four test sets of reference alignments: BAliBASE, SABmark, SMART and a new benchmark, PREFAB. MUSCLE achieves the highest, or joint highest, rank in accuracy on each of these sets. Without refinement, MUSCLE achieves average accuracy statistically indistinguishable from T-Coffee and MAFFT, and is the fastest of the tested methods for large numbers of sequences, aligning 5000 sequences of average length 350 in 7 min on a current desktop computer. The MUSCLE program, source code and PREFAB test data are freely available at http://www.drive5. com/muscle.
37,524 citations
"The genome of the leaf-cutting ant ..." refers methods in this paper
...After clustering, we performed multiple alignments of protein sequences for each gene family using MUSCLE (Edgar 2004) and reverse translated the protein alignments to CDS alignments....
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...Phylogenetic trees and gene family expansion/contraction To generate the overall phylogeny of the six Hymenopteran genomes and D. melanogaster, fourfold degenerate (FFD) sites were extracted from MUSCLE alignments of 1995 single-copy gene families and merged into one alignment....
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TL;DR: The goal of the Gene Ontology Consortium is to produce a dynamic, controlled vocabulary that can be applied to all eukaryotes even as knowledge of gene and protein roles in cells is accumulating and changing.
Abstract: Genomic sequencing has made it clear that a large fraction of the genes specifying the core biological functions are shared by all eukaryotes. Knowledge of the biological role of such shared proteins in one organism can often be transferred to other organisms. The goal of the Gene Ontology Consortium is to produce a dynamic, controlled vocabulary that can be applied to all eukaryotes even as knowledge of gene and protein roles in cells is accumulating and changing. To this end, three independent ontologies accessible on the World-Wide Web (http://www.geneontology.org) are being constructed: biological process, molecular function and cellular component.
35,225 citations
"The genome of the leaf-cutting ant ..." refers methods in this paper
...Gene Ontology (GO) (Ashburner et al. 2000) IDs for each gene were obtained from the corresponding InterPro entry....
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TL;DR: The Kyoto Encyclopedia of Genes and Genomes (KEGG) as discussed by the authors is a knowledge base for systematic analysis of gene functions in terms of the networks of genes and molecules.
Abstract: Kyoto Encyclopedia of Genes and Genomes (KEGG) is a knowledge base for systematic analysis of gene functions in terms of the networks of genes and molecules. The major component of KEGG is the PATHWAY database that consists of graphical diagrams of biochemical pathways including most of the known metabolic pathways and some of the known regulatory pathways. The pathway information is also represented by the ortholog group tables summarizing orthologous and paralogous gene groups among different organisms. KEGG maintains the GENES database for the gene catalogs of all organisms with complete genomes and selected organisms with partial genomes, which are continuously re-annotated, as well as the LIGAND database for chemical compounds and enzymes. Each gene catalog is associated with the graphical genome map for chromosomal locations that is represented by Java applet. In addition to the data collection efforts, KEGG develops and provides various computational tools, such as for reconstructing biochemical pathways from the complete genome sequence and for predicting gene regulatory networks from the gene expression profiles. The KEGG databases are daily updated and made freely available (http://www.genome.ad.jp/kegg/).
24,024 citations
TL;DR: Bowtie extends previous Burrows-Wheeler techniques with a novel quality-aware backtracking algorithm that permits mismatches and can be used simultaneously to achieve even greater alignment speeds.
Abstract: Bowtie is an ultrafast, memory-efficient alignment program for aligning short DNA sequence reads to large genomes. For the human genome, Burrows-Wheeler indexing allows Bowtie to align more than 25 million reads per CPU hour with a memory footprint of approximately 1.3 gigabytes. Bowtie extends previous Burrows-Wheeler techniques with a novel quality-aware backtracking algorithm that permits mismatches. Multiple processor cores can be used simultaneously to achieve even greater alignment speeds. Bowtie is open source http://bowtie.cbcb.umd.edu.
20,335 citations
"The genome of the leaf-cutting ant ..." refers methods in this paper
...Genome Research 1345 www.genome.org Known and putative miRNAs were aligned to the genome assembly using Bowtie (Langmead et al. 2009), allowing one mismatch....
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