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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2011
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oai:doaj.org-article:3b4c4017bcf347d99a4538cad73f59682021-11-18T06:17:43ZThe evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri.1553-73901553-740410.1371/journal.pgen.1001314https://doaj.org/article/3b4c4017bcf347d99a4538cad73f59682011-02-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21379339/pdf/?tool=EBIhttps://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Recent 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.Steven A FreseAndrew K BensonGerald W TannockDiane M LoachJaehyoung KimMin ZhangPhaik Lyn OhNicholas C K HengPrabhu B PatilNathalie JugeDonald A MackenzieBruce M PearsonAlla LapidusEileen DalinHope TiceEugene GoltsmanMiriam LandLoren HauserNatalia IvanovaNikos C KyrpidesJens WalterPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 7, Iss 2, p e1001314 (2011) |
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DOAJ |
| collection |
DOAJ |
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EN |
| topic |
Genetics QH426-470 |
| spellingShingle |
Genetics QH426-470 Steven A Frese Andrew K Benson Gerald W Tannock Diane M Loach Jaehyoung Kim Min Zhang Phaik Lyn Oh Nicholas C K Heng Prabhu B Patil Nathalie Juge Donald A Mackenzie Bruce M Pearson Alla Lapidus Eileen Dalin Hope Tice Eugene Goltsman Miriam Land Loren Hauser Natalia Ivanova Nikos C Kyrpides Jens Walter The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. |
| description |
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. |
| format |
article |
| author |
Steven A Frese Andrew K Benson Gerald W Tannock Diane M Loach Jaehyoung Kim Min Zhang Phaik Lyn Oh Nicholas C K Heng Prabhu B Patil Nathalie Juge Donald A Mackenzie Bruce M Pearson Alla Lapidus Eileen Dalin Hope Tice Eugene Goltsman Miriam Land Loren Hauser Natalia Ivanova Nikos C Kyrpides Jens Walter |
| author_facet |
Steven A Frese Andrew K Benson Gerald W Tannock Diane M Loach Jaehyoung Kim Min Zhang Phaik Lyn Oh Nicholas C K Heng Prabhu B Patil Nathalie Juge Donald A Mackenzie Bruce M Pearson Alla Lapidus Eileen Dalin Hope Tice Eugene Goltsman Miriam Land Loren Hauser Natalia Ivanova Nikos C Kyrpides Jens Walter |
| author_sort |
Steven A Frese |
| title |
The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. |
| title_short |
The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. |
| title_full |
The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. |
| title_fullStr |
The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. |
| title_full_unstemmed |
The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. |
| title_sort |
evolution of host specialization in the vertebrate gut symbiont lactobacillus reuteri. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2011 |
| url |
https://doaj.org/article/3b4c4017bcf347d99a4538cad73f5968 |
| work_keys_str_mv |
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