The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri
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 evolutio...
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| Published in: | PLoS genetics Vol. 7; no. 2; p. e1001314 |
|---|---|
| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Public Library of Science
01.02.2011
Public Library of Science (PLoS) |
| Subjects: | |
| ISSN: | 1553-7404, 1553-7390, 1553-7404 |
| Online Access: | Get full text |
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| 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. |
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| AbstractList | 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. 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.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. 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. The gastrointestinal microbiota of vertebrates is important for nutrient utilization, resistance against pathogens, and immune maturation of its host, but little is known about the evolutionary relationships between vertebrates and individual bacterial members of these communities. Here we provide robust evidence that the evolution of the gut symbiont Lactobacillus reuteri with vertebrates resulted in the emergence of host specialization. Genomic approaches using a combination of genome sequence comparisons and microarray analysis were used to identify the host-specific genome content in rodent and human strains and the evolutionary events that resulted in host adaptation. The study revealed divergent patterns of genome evolution in rodent and human lineages and a distinct genome inventory in host-restricted sub-populations of L. reuteri that reflected the niche characteristics in the gut of their particular vertebrate hosts. The ecological significance of representative rodent-specific genes was demonstrated in gnotobiotic mice. In conclusion, this work provided evidence that the vertebrate gut symbiont Lactobacillus reuteri, despite the likelihood of horizontal transmission, has remained stably associated with related groups of vertebrate hosts over evolutionary time and has evolved a lifestyle specialized to these host animals. 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. |
| Audience | Academic |
| Author | Pearson, Bruce M. Frese, Steven A. Hauser, Loren Lapidus, Alla Kim, Jaehyoung Tice, Hope Ivanova, Natalia Walter, Jens Zhang, Min Oh, Phaik Lyn Patil, Prabhu B. Land, Miriam Kyrpides, Nikos C. Tannock, Gerald W. Heng, Nicholas C. K. MacKenzie, Donald A. Loach, Diane M. Benson, Andrew K. Juge, Nathalie Goltsman, Eugene Dalin, Eileen |
| AuthorAffiliation | 5 Institute of Food Research, Norwich Research Park, Norwich, United Kingdom 7 Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America 1 Department of Food Science and Technology, University of Nebraska, Lincoln, Nebraska, United States of America 3 Sir John Walsh Research Institute (Faculty of Dentistry), University of Otago, Dunedin, New Zealand University of Toronto, Canada 4 Institute of Microbial Technology (IMTECH), Chandigarh, India 6 Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America 2 Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand |
| AuthorAffiliation_xml | – name: 1 Department of Food Science and Technology, University of Nebraska, Lincoln, Nebraska, United States of America – name: 7 Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America – name: 3 Sir John Walsh Research Institute (Faculty of Dentistry), University of Otago, Dunedin, New Zealand – name: 4 Institute of Microbial Technology (IMTECH), Chandigarh, India – name: 6 Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America – name: University of Toronto, Canada – name: 5 Institute of Food Research, Norwich Research Park, Norwich, United Kingdom – name: 2 Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand |
| Author_xml | – sequence: 1 givenname: Steven A. surname: Frese fullname: Frese, Steven A. – sequence: 2 givenname: Andrew K. surname: Benson fullname: Benson, Andrew K. – sequence: 3 givenname: Gerald W. surname: Tannock fullname: Tannock, Gerald W. – sequence: 4 givenname: Diane M. surname: Loach fullname: Loach, Diane M. – sequence: 5 givenname: Jaehyoung surname: Kim fullname: Kim, Jaehyoung – sequence: 6 givenname: Min surname: Zhang fullname: Zhang, Min – sequence: 7 givenname: Phaik Lyn surname: Oh fullname: Oh, Phaik Lyn – sequence: 8 givenname: Nicholas C. K. surname: Heng fullname: Heng, Nicholas C. K. – sequence: 9 givenname: Prabhu B. surname: Patil fullname: Patil, Prabhu B. – sequence: 10 givenname: Nathalie surname: Juge fullname: Juge, Nathalie – sequence: 11 givenname: Donald A. surname: MacKenzie fullname: MacKenzie, Donald A. – sequence: 12 givenname: Bruce M. surname: Pearson fullname: Pearson, Bruce M. – sequence: 13 givenname: Alla surname: Lapidus fullname: Lapidus, Alla – sequence: 14 givenname: Eileen surname: Dalin fullname: Dalin, Eileen – sequence: 15 givenname: Hope surname: Tice fullname: Tice, Hope – sequence: 16 givenname: Eugene surname: Goltsman fullname: Goltsman, Eugene – sequence: 17 givenname: Miriam surname: Land fullname: Land, Miriam – sequence: 18 givenname: Loren surname: Hauser fullname: Hauser, Loren – sequence: 19 givenname: Natalia surname: Ivanova fullname: Ivanova, Natalia – sequence: 20 givenname: Nikos C. surname: Kyrpides fullname: Kyrpides, Nikos C. – sequence: 21 givenname: Jens surname: Walter fullname: Walter, Jens |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21379339$$D View this record in MEDLINE/PubMed https://www.osti.gov/biblio/1007840$$D View this record in Osti.gov |
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| Copyright | COPYRIGHT 2011 Public Library of Science This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2011 2011 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Frese SA, Benson AK, Tannock GW, Loach DM, Kim J, et al. (2011) The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri. PLoS Genet 7(2): e1001314. doi:10.1371/journal.pgen.1001314 |
| Copyright_xml | – notice: COPYRIGHT 2011 Public Library of Science – notice: This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2011 – notice: 2011 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Frese SA, Benson AK, Tannock GW, Loach DM, Kim J, et al. (2011) The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri. PLoS Genet 7(2): e1001314. doi:10.1371/journal.pgen.1001314 |
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| SubjectTerms | Animals BASIC BIOLOGICAL SCIENCES BIOLOGY Colleges & universities Comparative analysis Evolution Evolution, Molecular Evolutionary Biology/Evolutionary Ecology Evolutionary Biology/Genomics Evolutionary Biology/Microbial Evolution and Genomics Experiments GASTROINTESTINAL TRACT Gastrointestinal Tract - microbiology GENERAL AND MISCELLANEOUS//MATHEMATICS, COMPUTING, AND INFORMATION SCIENCE GENES Genetic aspects Genetic Fitness Genetics and Genomics/Comparative Genomics Genetics and Genomics/Gene Function Genetics and Genomics/Microbial Evolution and Genomics Genome, Bacterial - genetics Genomes Genomics Host Specificity - genetics Host-bacteria relationships Humans INACTIVATION LACTOBACILLUS Limosilactobacillus reuteri - genetics MICE Microbiology Microbiology/Microbial Evolution and Genomics Microbiota (Symbiotic organisms) Natural history PLASTICITY Polymerase Chain Reaction Proteins Reproducibility of Results Rodentia - microbiology RODENTS Specialization Species Specificity SPECIFICITY STRAINS SYMBIOSIS Symbiosis - genetics VERTEBRATES Vertebrates - microbiology |
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| Title | The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri |
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