The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri

Authors

Steven A. Frese, University of Nebraska-LincolnFollow
Andrew K. Benson, University of Nebraska - LincolnFollow
Gerald W. Tannock, University of Otago, Dunedin, New Zealand
Diane M. Loach, University of Otago, Dunedin, New Zealand,
Jaehyoung Kim, University of Nebraska-Lincoln
Min Zhang, University of Nebraska-Lincoln
Phaik Lyn Oh, University of Nebraska-Lincoln
Nicholas C. K. Heng, University of Otago, Dunedin, New Zealand
Prabhu B. Patil, Institute of Microbial Technology (IMTECH), Chandigarh, India
Nathalie Juge, Institute of Food Research, Norwich, UK
Donald A. MacKenzie, Institute of Food Research, Norwich, UKFollow
Bruce M. Pearson, Institute of Food Research, Norwich, UK
Alla Lapidus, Department of Energy Joint Genome Institute, Walnut Creek, California
Eileen Dalin, Department of Energy Joint Genome Institute, Walnut Creek, California
Hope Tice, Department of Energy Joint Genome Institute, Walnut Creek, California
Eugene Goltsman, Department of Energy Joint Genome Institute, Walnut Creek, California
Miriam Land, Oak Ridge National Laboratory, Oak Ridge, Tennessee
Loren Hauser, Oak Ridge National Laboratory, Oak Ridge, Tennessee
Natalia Ivanova, Department of Energy Joint Genome Institute, Walnut Creek, California
Nikos C. Kyrpides, Department of Energy Joint Genome Institute, Walnut Creek, California
Jens Walter, University of Nebraska-LincolnFollow

Date of this Version

2011

Document Type

Article

Citation

PLoS Genet 7(2): e1001314. doi:10.1371/journal.pgen.1001314

Comments

Public domain article.

Abstract

Recent research has provided mechanistic insight into the important contributions of the gut microbiota to vertebrate biology, but questions remain about the evolutionary processes that have shaped this symbiosis. In the present study, we showed in experiments with gnotobiotic mice that the evolution of Lactobacillus reuteri with rodents resulted in the emergence of host specialization. To identify genomic events marking adaptations to the murine host, we compared the genome of the rodent isolate L. reuteri 100-23 with that of the human isolate L. reuteri F275, and we identified hundreds of genes that were specific to each strain. In order to differentiate true host-specific genome content from strain-level differences, comparative genome hybridizations were performed to query 57 L. reuteri strains originating from six different vertebrate hosts in combination with genome sequence comparisons of nine strains encompassing five phylogenetic lineages of the species. This approach revealed that rodent strains, although showing a high degree of genomic plasticity, possessed a specific genome inventory that was rare or absent in strains from other vertebrate hosts. The distinct genome content of L. reuteri lineages reflected the niche characteristics in the gastrointestinal tracts of their respective hosts, and inactivation of seven out of eight representative rodent-specific genes in L. reuteri 100-23 resulted in impaired ecological performance in the gut of mice. The comparative genomic analyses suggested fundamentally different trends of genome evolution in rodent and human L. reuteri populations, with the former possessing a large and adaptable pan-genome while the latter being subjected to a process of reductive evolution. In conclusion, this study provided experimental evidence and a molecular basis for the evolution of host specificity in a vertebrate gut symbiont, and it identified genomic events that have shaped this process.