High-quality functional genome annotation through an intercampus competition initiative

Ensuring high-quality functional annotations in newly sequenced genomes has become a fundamental problem in next-generation sequencing genomics. This problem takes additional relevance in bacteriophage genomics, where well-annotated reference genomes are scarce and often highly diverged from newly sequenced genomes. This makes automated annotation pipelines especially prone to introduce and propagate functional annotation errors, devaluing the contribution of sequencing projects to the understanding of bacteriophage biology and decreasing the likelihood that novel genetic mechanisms with industrial and clinical application can be mined from the extremely diverse genetic repertoire of bacteriophage genomes. Genome annotation by expert biocurators ensures high-quality annotations, but such approaches are hard to scale and raise financial sustainability issues. Here we show how undergraduate biology courses devoted to genome annotation can be leveraged to generate high-quality functional annotations of bacteriophage genomes by integrating targeted training within the framework of an intercampus annotation competition. Students receive advanced training on biological ontologies, orthology assessment methods, biocuration standards and critical reading of scientific manuscripts. Working in small teams, students then participate in the Community Assessment of Community Annotation with Ontologies (CACAO) intercampus competition, generating Gene Ontology (GO) annotations of bacteriophage and bacterial gene products and challenging the accuracy of annotations made by other teams in a pre-established set of innings for annotation, challenge and revision. Revised annotations are reviewed by an expert panel before submission to the Gene Ontology Consortium. This approach yields tangible benefits on many fronts. Students develop critical reading skills, get exposed to key concepts in genome biology and obtain essential hands-on experience on the use of ontologies and bioinformatics methods to assess orthology, synteny and other genetic features. Team-work in a competitive framework and intercampus rivalry motivate students to improve the accuracy of their annotations, leading to high-quality functional annotations on both reference and newly sequenced bacteriophage genomes.