Exchanging DNA Here, There, and Everywhere

Lateral DNA Transfer: Mechanisms and Consequences By Frederic Bushman Cold Spring Harbor, NY: Cold Spring Harbor Press (2002). 448 pp. $59.00Monsieur Jordan: Par ma foi! il y a plus de quarante ans que je dis de la prose sans que j'en susse rien, et je vous suis le plus oblige du monde de m'avoir appris cela.—Moliere, Le Bourgeois Gentilhomme One of the most fascinating cases of naturally occurring genetic engineering is the bacteria-promoted crown gall disease of plants. This disease occurs when the soil bacterium Agrobacterium tumefaciens infects a wounded plant and introduces into its nuclear genome a DNA segment encoding proteins that promote the formation of swellings (i.e., the crown galls) that synthesize nutrients that can be used only by the infecting bacterial species. By incorporating foreign genes into the DNA segment transferred by A. tumefaciens, scientists can modify plant cells, which results in the development of crop plants exhibiting novel traits.Two of the lessons that we have learned from the sequencing of whole genomes are the following: first, many of the characteristics that distinguish bacterial species, such as virulence potential and metabolic abilities, are encoded within species-specific regions of the genome. And second, in contrast to bacterial genomes, which devote approximately 90% of their content to coding regions, only 1.5% of the human genome is coding DNA, the remaining “junk” being made up of transposons and viruses. The extent to which different eukaryotic organisms have acquired such elements may help explain the C-value paradox—the observation that genome size does not necessarily correlate with organism complexity (for example, the human genome is 30 times bigger than that of baker's yeast, yet 20 times smaller than the genome of certain amoebas).Numerous biological phenomena, including the development of tumors in animals and plants, the spread of antibiotic resistance determinants in bacteria, and the abnormalities resulting from certain types of crosses in insects, result from lateral DNA transfer. Also referred to as horizontal gene transfer, lateral DNA transfer is the movement of DNA from one organism to another in which it becomes stably incorporated. The widespread nature of lateral DNA transfer and the realization that DNA can move from one location to another within an organism lead to the view that genomes are in a state of flux. However, this view was not readily accepted as Barbara McClintock was not awarded the Nobel Prize for her discovery of “mobile genetic elements” in plants until 1983, a belated recognition of work she had conducted in the 1940s which was fully appreciated only when transposable elements were rediscovered in bacteria. Coincidentally, 1983 also marked the publication of Mobile Genetic Elements, the first comprehensive discussion of DNA movement within and among organisms, which was written by several experts and superbly edited by Jim Shapiro.The scope and consequences of lateral DNA transfer have been increasingly appreciated since the publication of Mobile Genetic Elements. Thus, it was comforting to read Frederic Bushman's marvelous new book, Lateral DNA Transfer: Mechanisms and Consequences. Bushman uses less than 450 pages to teach us not only about the molecular bases for many of the genetic discoveries of the 1980s and 1990s, but also about the impact of lateral DNA transfer in infectious diseases, bacterial speciation, and the evolution of eukaryotic organisms. Lateral DNA Transfer discusses several additional topics, including the different families of transposons and mechanisms of transposition, the molecular evidence for the endosymbiotic theory, and the hypothesis of a transposon being the progenitor of the vertebrate immune system.Bushman's book is organized in 14 chapters, beginning with an introduction and a brief crash course on molecular biology, and concluding with the general principles governing lateral DNA transfer and its evolutionary implications. Three chapters are devoted to horizontal gene transfer in prokaryotes, including a genomic-based one analyzing rates of transfer, discussing why bacterial genes are organized in operons, and raising issues pertaining to bacterial phylogeny. Six chapters analyze DNA transfer in eukaryotes, emphasizing retroviruses and the use of genomic data to infer transfer frequencies in different organisms. The two remaining chapters cover gene exchange across domains of life and the regulatory mechanisms governing DNA transfer. Each chapter begins with a discussion of the biological context of the topic, includes excellent illustrations, provides current references from the primary literature, and concludes with a brief summary. Most importantly, the writing is clear and to the point, allowing reading of the chapters (or sections of them) without following the original order.It has now become clear that lateral DNA transfer has played and continues to play a major role in shaping genomes. Lateral DNA Transfer constitutes a great effort to put under one umbrella a variety of topics pertaining to genome evolution. Moreover, it provides a molecular genetic framework to understand the current technological applications of gene transfer including gene therapy, crop improvement, and control of insect populations.Most readers will find plenty of new information in Lateral DNA Transfer. For example, they will learn that the estimated frequency of gene transfer between organisms in the oceans is twenty billion times per second. On the other hand, many of the topics discussed by Bushman might not be new for other readers. Yet, these topics are presented with a different spin that makes us feel like a molecular biologist version of the bourgeois gentleman Monsieur Jordan: that we have been investigating/reading about/exploring lateral DNA transfer and we did not even know it.