Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes

Julie C. Dunning Hotopp,^1* Michael E. Clark,^2* Deodoro C. S. G. Oliveira,² Jeremy M. Foster,³ Peter Fischer,⁴ Mónica C. Muñoz Torres,⁵ Jonathan D. Giebel,² Nikhil Kumar,¹ Nadeeza Ishmael,¹ Shiliang Wang,¹ Jessica Ingram,³ Rahul V. Nene,¹ Jessica Shepard,^1|| Jeffrey Tomkins,⁵ Stephen Richards,⁶ David J. Spiro,¹ Elodie Ghedin,^1,7 Barton E. Slatko,³ Hervé Tettelin,^1¶ John H. Werren^2¶

Although common among bacteria, lateral gene transfer—the movement of genes between distantly related organisms—is thought to occur only rarely between bacteria and multicellular eukaryotes. However, the presence of endosymbionts, such as Wolbachia pipientis, within some eukaryotic germlines may facilitate bacterial gene transfers to eukaryotic host genomes. We therefore examined host genomes for evidence of gene transfer events from Wolbachia bacteria to their hosts. We found and confirmed transfers into the genomes of four insect and four nematode species that range from nearly the entire Wolbachia genome (>1 megabase) to short (<500 base pairs) insertions. Potential Wolbachia-to-host transfers were also detected computationally in three additional sequenced insect genomes. We also show that some of these inserted Wolbachia genes are transcribed within eukaryotic cells lacking endosymbionts. Therefore, heritable lateral gene transfer occurs into eukaryotic hosts from their prokaryote symbionts, potentially providing a mechanism for acquisition of new genes and functions.

¹ The Institute for Genomic Research, J. Craig Venter Institute, 9712 Medical Center Drive, Rockville, MD 20850, USA.
² Department of Biology, University of Rochester, Rochester, NY 14627, USA.
³ Molecular Parasitology Division, New England Biolabs Incorporated, 240 County Road, Ipswich, MA 01938, USA.
⁴ Department of Internal Medicine, Infectious Diseases Division, Washington University School of Medicine, St. Louis, MO 63110, USA.
⁵ Clemson University Genomics Institute, 304 BRC, 51 New Cherry Street, Clemson, SC 29634, USA.
⁶ Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX 77030, USA.
⁷ Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261, USA.

^* These authors contributed equally to this work.

Present address: Institute for Genome Sciences, University of Maryland School of Medicine, Health Sciences Facility II, Room S-445, 20 Penn Street, Baltimore, MD 21201, USA.

Present address:BrownUniversity,Providence,RI02912,USA.

^|| Present address: Pace University, New York, NY 10038, USA.

^¶ These authors contributed equally to this work.

To whom correspondence should be addressed. E-mail: jhotopp{at}som.umaryland.edu