Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility

Patrick Chain1,2,3, Vincent J. Denef4,5,6, Robert M. Kelly4,7, Lisa M. Vergez1,3,8, Loreine Agulló9, Valeria Latorre Reyes10,9,11, Loren Hauser12, Macarena Córdova9, Luis Gómez9, Myriam González9, Miriam Land12, Victoria Lao1, Frank W. Larimer12, John J. LiPuma13, Eshwar Mahenthiralingam14, Stephanie Malfatti1,3,8, Christopher J. Marx15, Jacob Parnell4, Alban Ramette16,17, Daniel S. Rokhsar3,18, Michael Seeger9, Daryl J. Smith19, Theodore Spilker13, Woo Jun Sul4, Tsoĭ Tv4, Luke E. Ulrich20, Igor B. Zhulin20, James M. Tiedje4,21
1Biosciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA 94550;
2Center for Microbial Ecology Michigan State University, East Lansing, MI 48824, USA
3Joint Genome Institute, Walnut Creek, CA 94598;
4Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824.
5Department of Bioscience Engineering, Universiteit Gent, 9000 Gent, Belgium;
6Department of Earth and Planetary Sciences, University of California, Berkeley, CA 94720; and
7Department of Civil and Environmental Engineering, Massachussets Institute of Technology, Boston, MA 02139;
8U.S. Department of Energy
9Nucleus Millennium of Microbial Ecology and Environmental Microbiology and Biotechnology, Universidad Técnica Federico Santa María, Casilla 110-V, Valparaíso, Chile;
10Departamento de Ciencias y Recursos Naturales, Universidad de Magallanes, Casilla 113-D, Punta Arenas, Chile
11University of California at Berkeley
12Oak Ridge National Laboratory, Oak Ridge, TN 37831
13Department of Pediatrics and Communicable Diseases, University of Michigan, Ann Arbor, MI 48109
14School of Biosciences, Cardiff University, Cardiff CF10 3TL, Wales, United Kingdom;
15Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
16HGF MPG Joint Research Group for Deep Sea Ecology & Technology, Max Planck Institute for Marine Microbiology, Max Planck Society
17Max-Planck-Institute for Marine Microbiology, 28359 Bremen, Germany;
18U.S. Dept. Of Energy
19Life Sciences Institute, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
20Joint Institute for Computational Sciences, University of Tennessee–Oak Ridge National Laboratory, Oak Ridge, TN 37831;
21Microbiology and Molecular Genetics

Tóm tắt

Burkholderia xenovorans LB400 (LB400), a well studied, effective polychlorinated biphenyl-degrader, has one of the two largest known bacterial genomes and is the first nonpathogenic Burkholderia isolate sequenced. From an evolutionary perspective, we find significant differences in functional specialization between the three replicons of LB400, as well as a more relaxed selective pressure for genes located on the two smaller vs. the largest replicon. High genomic plasticity, diversity, and specialization within the Burkholderia genus are exemplified by the conservation of only 44% of the genes between LB400 and Burkholderia cepacia complex strain 383. Even among four B. xenovorans strains, genome size varies from 7.4 to 9.73 Mbp. The latter is largely explained by our findings that >20% of the LB400 sequence was recently acquired by means of lateral gene transfer. Although a range of genetic factors associated with in vivo survival and intercellular interactions are present, these genetic factors are likely related to niche breadth rather than determinants of pathogenicity. The presence of at least eleven “central aromatic” and twenty “peripheral aromatic” pathways in LB400, among the highest in any sequenced bacterial genome, supports this hypothesis. Finally, in addition to the experimentally observed redundancy in benzoate degradation and formaldehyde oxidation pathways, the fact that 17.6% of proteins have a better LB400 paralog than an ortholog in a different genome highlights the importance of gene duplication and repeated acquirement, which, coupled with their divergence, raises questions regarding the role of paralogs and potential functional redundancies in large-genome microbes.

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