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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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Rodent-specific large surface proteins of L. reuteri 100-23.The architecture of large surface proteins (>750 aa) specific to rodent strains when compared to human isolates of the MLSA lineage II. Functional domains of each protein are shown as indicated and to scale.
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pgen-1001314-g005: Rodent-specific large surface proteins of L. reuteri 100-23.The architecture of large surface proteins (>750 aa) specific to rodent strains when compared to human isolates of the MLSA lineage II. Functional domains of each protein are shown as indicated and to scale.

Mentions: Eleven large (>750 aa) surface proteins were detected in rodent strains that were very rare in isolates of pigs and poultry and absent in human isolates of MLSA lineage II (Figure 3). The characteristics of these proteins are described in Table 3 and their schematic representation is shown in Figure 5. Most of the surface proteins are predicted to be involved in epithelial adhesion and biofilm formation. Six proteins (Lr_69656, Lr_70131, Lr_70134, Lr_70135, Lr_70581, Lr_71380) contained putative mucin-binding MucBP domains (Pfam PF06458) and other domains involved in extracellular matrix binding. Additional domains detected included a glycosyltransferase (family 68) domain in a predicted levansucrase (Lr_71010), and a putative IgA-specific protease (Lr_69916).


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)

Rodent-specific large surface proteins of L. reuteri 100-23.The architecture of large surface proteins (>750 aa) specific to rodent strains when compared to human isolates of the MLSA lineage II. Functional domains of each protein are shown as indicated and to scale.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g005: Rodent-specific large surface proteins of L. reuteri 100-23.The architecture of large surface proteins (>750 aa) specific to rodent strains when compared to human isolates of the MLSA lineage II. Functional domains of each protein are shown as indicated and to scale.
Mentions: Eleven large (>750 aa) surface proteins were detected in rodent strains that were very rare in isolates of pigs and poultry and absent in human isolates of MLSA lineage II (Figure 3). The characteristics of these proteins are described in Table 3 and their schematic representation is shown in Figure 5. Most of the surface proteins are predicted to be involved in epithelial adhesion and biofilm formation. Six proteins (Lr_69656, Lr_70131, Lr_70134, Lr_70135, Lr_70581, Lr_71380) contained putative mucin-binding MucBP domains (Pfam PF06458) and other domains involved in extracellular matrix binding. Additional domains detected included a glycosyltransferase (family 68) domain in a predicted levansucrase (Lr_71010), and a putative IgA-specific protease (Lr_69916).

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