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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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Analysis of genome content by reference microarray.The dendrogram is derived from UPGMA analysis of binary data generated from 57 strains of Lactobacillus reuteri. Bootstrap scores, using 10,000 repetitions of a UPGMA search, are shown on nodes scoring >50%. Each strain is color coded by host, and affiliation to MLSA lineages of each strain is indicated. MARKFIND was used to identify gene polymorphisms specific to human (MLSA lineage II) and rodent strains (mostly MLSA lineages I and III), which clustered in the dendrogram. The leaves of human (lineage II) and rodent strains, which have been used for comparisons by MARKFIND, are colored blue and red, respectively. The two reference strains, 100-23 and F275, are labeled by a red and a blue circle, respectively. Vertical rectangles to the right depict polymorphisms present in a given strain sorted by the MARKFIND program. Those polymorphisms conserved within all members of a lineage and absent in the other lineage are colored red. Genes that are lineage-specific but non conserved are colored green (polyphyletic) or yellow (monophyletic). Polymorphisms that are not lineage specific are not shown.
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pgen-1001314-g002: Analysis of genome content by reference microarray.The dendrogram is derived from UPGMA analysis of binary data generated from 57 strains of Lactobacillus reuteri. Bootstrap scores, using 10,000 repetitions of a UPGMA search, are shown on nodes scoring >50%. Each strain is color coded by host, and affiliation to MLSA lineages of each strain is indicated. MARKFIND was used to identify gene polymorphisms specific to human (MLSA lineage II) and rodent strains (mostly MLSA lineages I and III), which clustered in the dendrogram. The leaves of human (lineage II) and rodent strains, which have been used for comparisons by MARKFIND, are colored blue and red, respectively. The two reference strains, 100-23 and F275, are labeled by a red and a blue circle, respectively. Vertical rectangles to the right depict polymorphisms present in a given strain sorted by the MARKFIND program. Those polymorphisms conserved within all members of a lineage and absent in the other lineage are colored red. Genes that are lineage-specific but non conserved are colored green (polyphyletic) or yellow (monophyletic). Polymorphisms that are not lineage specific are not shown.

Mentions: CGH patterns were analyzed using the MARKFIND program [45], which performs a cluster analysis based on genome polymorphisms by the unweighted pair-group method with arithmetic means (UPGMA). As shown in Figure 2, the phylogeny inferred from the genome polymorphisms reflected both host origin and MLSA typing. The rodent strains formed one cluster comprised of three sub-groups (i, ii, and iii), with i and ii corresponding to MLSA lineages III and I, respectively. The human and poultry isolates that belong to the MLSA lineage VI also formed one separate group with CGH. The human strains from MLSA cluster II formed an isolated cluster that grouped distantly from all other L. reuteri strains, which is indicative of markedly different genome content (Figure 2). Thus, although the topologies of the dendrograms inferred from gene polymorphisms and MLSA sequences were different, both methods resulted in trees with host-specific phylogenetic clusters that were congruent. This indicates that L. reuteri has diverged into genetically and ecologically cohesive subpopulations (ecotypes) whose gene content reflects particular host niches.


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)

Analysis of genome content by reference microarray.The dendrogram is derived from UPGMA analysis of binary data generated from 57 strains of Lactobacillus reuteri. Bootstrap scores, using 10,000 repetitions of a UPGMA search, are shown on nodes scoring >50%. Each strain is color coded by host, and affiliation to MLSA lineages of each strain is indicated. MARKFIND was used to identify gene polymorphisms specific to human (MLSA lineage II) and rodent strains (mostly MLSA lineages I and III), which clustered in the dendrogram. The leaves of human (lineage II) and rodent strains, which have been used for comparisons by MARKFIND, are colored blue and red, respectively. The two reference strains, 100-23 and F275, are labeled by a red and a blue circle, respectively. Vertical rectangles to the right depict polymorphisms present in a given strain sorted by the MARKFIND program. Those polymorphisms conserved within all members of a lineage and absent in the other lineage are colored red. Genes that are lineage-specific but non conserved are colored green (polyphyletic) or yellow (monophyletic). Polymorphisms that are not lineage specific are not shown.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g002: Analysis of genome content by reference microarray.The dendrogram is derived from UPGMA analysis of binary data generated from 57 strains of Lactobacillus reuteri. Bootstrap scores, using 10,000 repetitions of a UPGMA search, are shown on nodes scoring >50%. Each strain is color coded by host, and affiliation to MLSA lineages of each strain is indicated. MARKFIND was used to identify gene polymorphisms specific to human (MLSA lineage II) and rodent strains (mostly MLSA lineages I and III), which clustered in the dendrogram. The leaves of human (lineage II) and rodent strains, which have been used for comparisons by MARKFIND, are colored blue and red, respectively. The two reference strains, 100-23 and F275, are labeled by a red and a blue circle, respectively. Vertical rectangles to the right depict polymorphisms present in a given strain sorted by the MARKFIND program. Those polymorphisms conserved within all members of a lineage and absent in the other lineage are colored red. Genes that are lineage-specific but non conserved are colored green (polyphyletic) or yellow (monophyletic). Polymorphisms that are not lineage specific are not shown.
Mentions: CGH patterns were analyzed using the MARKFIND program [45], which performs a cluster analysis based on genome polymorphisms by the unweighted pair-group method with arithmetic means (UPGMA). As shown in Figure 2, the phylogeny inferred from the genome polymorphisms reflected both host origin and MLSA typing. The rodent strains formed one cluster comprised of three sub-groups (i, ii, and iii), with i and ii corresponding to MLSA lineages III and I, respectively. The human and poultry isolates that belong to the MLSA lineage VI also formed one separate group with CGH. The human strains from MLSA cluster II formed an isolated cluster that grouped distantly from all other L. reuteri strains, which is indicative of markedly different genome content (Figure 2). Thus, although the topologies of the dendrograms inferred from gene polymorphisms and MLSA sequences were different, both methods resulted in trees with host-specific phylogenetic clusters that were congruent. This indicates that L. reuteri has diverged into genetically and ecologically cohesive subpopulations (ecotypes) whose gene content reflects particular host niches.

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