The network of life: genome beginnings and evolution
Mark A. Ragan1,*, James O. McInerney2 and James A. Lake3,4,5
+Author Affiliations
1Institute for Molecular Bioscience, and ARC Centre of Excellence in Bioinformatics, The University of Queensland, Brisbane, Australia
2Department of Biology, The National University of Ireland, Maynooth, Maynooth Co. Kildare, Ireland
3Department of MCD Biology
4Department of Human Genetics
5Molecular Biology Institute, University of California, Los Angeles, CA, USA
*Author for correspondence (m.ragan@imb.uq.edu.au).
genome origins lateral genetic transfer tree of life network of life evolution of viruses evolution of developmental pathways
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The genome sequence is an icon of early twenty-first century biology. Genomes of nearly 2000 cellular organisms, and from many thousands of organelles and viruses, are now in the public domain. For biological research in individual species, the genome sequence increasingly provides the common reference for the application of polymorphism, transcriptomic, proteomic and other genome-scale data to problems of development or disease. More recently, through metagenomic sequencing, the composition and function of ecosystems are being explored at the molecular level.
Genomes are now central to genetics, cell and developmental biology, molecular and systems biology, population biology and ecology.
At the same time, one cannot but be struck by the diversity of genomes, both across the living world and, in many cases, within genera or species. Whatever constraints may be imposed by their central role in genetics, functional and cell biology clearly do not stand in the way of genomes ranging in size over eight orders of magnitude and exhibiting remarkable diversity and variation in gene content, gene order and organization. Perhaps most unexpected of all is the substantial decoupling, now known in most, although not all, branches of organismal life, between the phylogenetic histories of individual gene families and what has generally been accepted to be the history of genomes and/or their cellular or organismal host lineages. The tree of life paradigm consolidated by Darwin's Origin of Species (1859), but itself arising from a much older tradition of natural history, seems likely to emerge, if at all, from the multi-genome era much more restricted in scope, and subject to many more qualifications, than could have been anticipated a dozen years ago.
The papers in this theme issue of Philosophical Transactions B present important perspectives on the origin and evolution of genomes. Key questions include genome beginnings: what preceded genomes? How were the first genomes organized, and according to what principles, by what mechanisms and along what paths did they begin to diversify? Our expert contributors explore genome diversity—among the deepest lineages, and from the highest taxon levels to intriguing individual species— discussing the processes that have shaped, and continue to shape, genomes of bacteria, archaebacteria and eukaryotes. A major theme is lateral (horizontal) genetic transmission, some (perhaps much) of which involves the abundant small elements that pervade the biosphere—viruses, plasmids, gene transfer agents—that can not only shuttle DNA among cellular organisms but also modify it in the process. Do the frequency and impact of lateral transfers on (many) genomes render the tree of life only an approximation—useful in some contexts, less so in others—or indeed is the tree of life paradigm now a barrier to a richer, more integrative understanding of life on Earth?
We have grouped these papers to reflect the chronology and significant evolutionary events in the origin and evolution of genomes. The emerging narrative is fresh with competing concepts and theories. In other words, in the field of genome evolution, the scientific process is alive and healthy.
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