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The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri.

Frese SA, Benson AK, Tannock GW, Loach DM, Kim J, Zhang M, Oh PL, Heng NC, Patil PB, Juge N, Mackenzie DA, Pearson BM, Lapidus A, Dalin E, Tice H, Goltsman E, Land M, Hauser L, Ivanova N, Kyrpides NC, Walter J - PLoS Genet. (2011)

Bottom Line: 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 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Food Science and Technology, University of Nebraska, Lincoln, Nebraska, United States of America.

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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Pair-wise genomic comparisons between L. reuteri strains 100-23 and F275.Linear genomic comparison of the chromosomes of 100-23 and F275 (using the sequence of JCM1112T). Both sequences are read left to right from the predicted origin of replication. Homologous regions within the two genomes identified by reciprocal BLASTN are indicated by red (same orientation) and blue (reverse orientation) bars. Putative horizontally acquired islands as identified by Alien_hunter (blue boxes), phage proteins (black boxes), transposases (orange boxes), and integrases (pink boxes) are indicated.
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pgen-1001314-g001: Pair-wise genomic comparisons between L. reuteri strains 100-23 and F275.Linear genomic comparison of the chromosomes of 100-23 and F275 (using the sequence of JCM1112T). Both sequences are read left to right from the predicted origin of replication. Homologous regions within the two genomes identified by reciprocal BLASTN are indicated by red (same orientation) and blue (reverse orientation) bars. Putative horizontally acquired islands as identified by Alien_hunter (blue boxes), phage proteins (black boxes), transposases (orange boxes), and integrases (pink boxes) are indicated.

Mentions: We used the Artemis Comparison Tool to localize strain specific genomic regions in L. reuteri 100-23 and F275 (Figure 1). The two genomes contained many regions of synteny, especially around the origin of replication. However, one major rearrangement and a major inversion were also present. The rearrangement was likely to have occurred in 100-23 as the F275 genome sequence shows greater synteny with the genome of the related species Lactobacillus fermentum (Figure S1), and it is therefore likely to reflect the ancestral structure. In addition, the inversion within the genome of 100-23 was rich in genetic elements (e.g. transposases), which may have caused the rearrangement through a recombination event (Figure 1). Many of the genes that were unique to 100-23 or F275 were clustered in genomic regions that were completely absent in the other strain. Several of these regions showed characteristics of genomic islands as they were associated with unusual sequence features such as low %GC content, atypical codon bias, mobile genetic elements (prophage related genes or putative IS elements/transposons), and they were predicted to be transferred by lateral gene transfer (LGT) using the software Alien_hunter. Several other regions were identified to be present in both genomes but differed significantly in terms of gene content. These regions coded for genes involved in the production of surface polysaccharides (SPS1 and SPS2) or contained putative prophages.


The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri.

Frese SA, Benson AK, Tannock GW, Loach DM, Kim J, Zhang M, Oh PL, Heng NC, Patil PB, Juge N, Mackenzie DA, Pearson BM, Lapidus A, Dalin E, Tice H, Goltsman E, Land M, Hauser L, Ivanova N, Kyrpides NC, Walter J - PLoS Genet. (2011)

Pair-wise genomic comparisons between L. reuteri strains 100-23 and F275.Linear genomic comparison of the chromosomes of 100-23 and F275 (using the sequence of JCM1112T). Both sequences are read left to right from the predicted origin of replication. Homologous regions within the two genomes identified by reciprocal BLASTN are indicated by red (same orientation) and blue (reverse orientation) bars. Putative horizontally acquired islands as identified by Alien_hunter (blue boxes), phage proteins (black boxes), transposases (orange boxes), and integrases (pink boxes) are indicated.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3040671&req=5

pgen-1001314-g001: Pair-wise genomic comparisons between L. reuteri strains 100-23 and F275.Linear genomic comparison of the chromosomes of 100-23 and F275 (using the sequence of JCM1112T). Both sequences are read left to right from the predicted origin of replication. Homologous regions within the two genomes identified by reciprocal BLASTN are indicated by red (same orientation) and blue (reverse orientation) bars. Putative horizontally acquired islands as identified by Alien_hunter (blue boxes), phage proteins (black boxes), transposases (orange boxes), and integrases (pink boxes) are indicated.
Mentions: We used the Artemis Comparison Tool to localize strain specific genomic regions in L. reuteri 100-23 and F275 (Figure 1). The two genomes contained many regions of synteny, especially around the origin of replication. However, one major rearrangement and a major inversion were also present. The rearrangement was likely to have occurred in 100-23 as the F275 genome sequence shows greater synteny with the genome of the related species Lactobacillus fermentum (Figure S1), and it is therefore likely to reflect the ancestral structure. In addition, the inversion within the genome of 100-23 was rich in genetic elements (e.g. transposases), which may have caused the rearrangement through a recombination event (Figure 1). Many of the genes that were unique to 100-23 or F275 were clustered in genomic regions that were completely absent in the other strain. Several of these regions showed characteristics of genomic islands as they were associated with unusual sequence features such as low %GC content, atypical codon bias, mobile genetic elements (prophage related genes or putative IS elements/transposons), and they were predicted to be transferred by lateral gene transfer (LGT) using the software Alien_hunter. Several other regions were identified to be present in both genomes but differed significantly in terms of gene content. These regions coded for genes involved in the production of surface polysaccharides (SPS1 and SPS2) or contained putative prophages.

Bottom Line: 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 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Food Science and Technology, University of Nebraska, Lincoln, Nebraska, United States of America.

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.

Show MeSH
Related in: MedlinePlus