Limits...
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.

Show MeSH

Related in: MedlinePlus

Ecological significance of rodent-specific genes for fitness of L. reuteri 100-23C in the mouse GIT.Competition between wild-type and mutant L. reuteri 100-23C strains in Lactobacillus-free mice. Mixtures of wild-type and mutant (1∶1) were used to inoculate mice, and the percentage of mutants in the total Lactobacillus population was determined after 7 days. The whiskers show the range of values obtained with different animals (n = 5–6), with the box indicating the 25th and 75th percentile. The bars in the boxes indicate median values. Mutants are listed by gene names; Lr_70770 (surface protein), Lr_70892 (SecA2 translocase), Lr_70430 (two-component system histidine kinase), Lr_70458 (ABC-type multidrug transport system), Lr_70532 (ABC-type transporter of TCS2), Lr_70890 (Asp2, involved in SecA2 transport system), Lr_70894 (SecY2), Lr_70902 (serine-rich surface protein).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3040671&req=5

pgen-1001314-g007: Ecological significance of rodent-specific genes for fitness of L. reuteri 100-23C in the mouse GIT.Competition between wild-type and mutant L. reuteri 100-23C strains in Lactobacillus-free mice. Mixtures of wild-type and mutant (1∶1) were used to inoculate mice, and the percentage of mutants in the total Lactobacillus population was determined after 7 days. The whiskers show the range of values obtained with different animals (n = 5–6), with the box indicating the 25th and 75th percentile. The bars in the boxes indicate median values. Mutants are listed by gene names; Lr_70770 (surface protein), Lr_70892 (SecA2 translocase), Lr_70430 (two-component system histidine kinase), Lr_70458 (ABC-type multidrug transport system), Lr_70532 (ABC-type transporter of TCS2), Lr_70890 (Asp2, involved in SecA2 transport system), Lr_70894 (SecY2), Lr_70902 (serine-rich surface protein).

Mentions: Although it is striking how gene content of L. reuteri lineages reflects niche characteristics in particular hosts, differences in gene frequencies within populations can arise not only through natural selection but also random genetic drift. In order to test whether the rodent specific genes were of ecological significance in the GIT of mice, we investigated the fitness of isogenic mutants of strain 100-23C in the gut of LF mice in competition with the parental strain. Eight genes representing major groups of genetic functions among the lineage-specific genes were selected for these experiments: Lr_70902 (serine-rich surface protein), Lr_70770 (putative adhesin), Lr_70892 (SecA2 translocase), Lr_70890 (Asp2, involved in SecA2 transport system), Lr_70894 (SecY2, involved in SecA2 transport system), Lr_70430 (two-component system histidine kinase), Lr_70458 (ABC-type multidrug transport system), Lr_70532 (ABC-type transporter of TCS2). This selection included sets of genes with high (Lr_70902, Lr_70770, Lr_70892, Lr_70890, Lr_70894, Lr_70532) and low conservation (Lr_70430, Lr_70458) among rodent strains. Further, it included genes with a variety of functions, such as adherence, secretion of surface proteins, and environmental sensing. As shown in Figure 7, when the parental strains and their mutant derivatives were introduced into LF mice, seven out of the eight mutants had impaired ecological fitness. The most significant defect in competitive fitness was caused through the inactivation of Lr_70890, Lr_70894, and Lr_70902, which are all associated with the secA2 operon. The only gene that did not contribute to ecological performance was Lr_70770, which encoded a putative adhesin. Given the large number of putative adhesins in the genome of L. reuteri 100-23 (Table 3), it is possible that redundancy exists in mechanisms that confer adherence.


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)

Ecological significance of rodent-specific genes for fitness of L. reuteri 100-23C in the mouse GIT.Competition between wild-type and mutant L. reuteri 100-23C strains in Lactobacillus-free mice. Mixtures of wild-type and mutant (1∶1) were used to inoculate mice, and the percentage of mutants in the total Lactobacillus population was determined after 7 days. The whiskers show the range of values obtained with different animals (n = 5–6), with the box indicating the 25th and 75th percentile. The bars in the boxes indicate median values. Mutants are listed by gene names; Lr_70770 (surface protein), Lr_70892 (SecA2 translocase), Lr_70430 (two-component system histidine kinase), Lr_70458 (ABC-type multidrug transport system), Lr_70532 (ABC-type transporter of TCS2), Lr_70890 (Asp2, involved in SecA2 transport system), Lr_70894 (SecY2), Lr_70902 (serine-rich surface protein).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g007: Ecological significance of rodent-specific genes for fitness of L. reuteri 100-23C in the mouse GIT.Competition between wild-type and mutant L. reuteri 100-23C strains in Lactobacillus-free mice. Mixtures of wild-type and mutant (1∶1) were used to inoculate mice, and the percentage of mutants in the total Lactobacillus population was determined after 7 days. The whiskers show the range of values obtained with different animals (n = 5–6), with the box indicating the 25th and 75th percentile. The bars in the boxes indicate median values. Mutants are listed by gene names; Lr_70770 (surface protein), Lr_70892 (SecA2 translocase), Lr_70430 (two-component system histidine kinase), Lr_70458 (ABC-type multidrug transport system), Lr_70532 (ABC-type transporter of TCS2), Lr_70890 (Asp2, involved in SecA2 transport system), Lr_70894 (SecY2), Lr_70902 (serine-rich surface protein).
Mentions: Although it is striking how gene content of L. reuteri lineages reflects niche characteristics in particular hosts, differences in gene frequencies within populations can arise not only through natural selection but also random genetic drift. In order to test whether the rodent specific genes were of ecological significance in the GIT of mice, we investigated the fitness of isogenic mutants of strain 100-23C in the gut of LF mice in competition with the parental strain. Eight genes representing major groups of genetic functions among the lineage-specific genes were selected for these experiments: Lr_70902 (serine-rich surface protein), Lr_70770 (putative adhesin), Lr_70892 (SecA2 translocase), Lr_70890 (Asp2, involved in SecA2 transport system), Lr_70894 (SecY2, involved in SecA2 transport system), Lr_70430 (two-component system histidine kinase), Lr_70458 (ABC-type multidrug transport system), Lr_70532 (ABC-type transporter of TCS2). This selection included sets of genes with high (Lr_70902, Lr_70770, Lr_70892, Lr_70890, Lr_70894, Lr_70532) and low conservation (Lr_70430, Lr_70458) among rodent strains. Further, it included genes with a variety of functions, such as adherence, secretion of surface proteins, and environmental sensing. As shown in Figure 7, when the parental strains and their mutant derivatives were introduced into LF mice, seven out of the eight mutants had impaired ecological fitness. The most significant defect in competitive fitness was caused through the inactivation of Lr_70890, Lr_70894, and Lr_70902, which are all associated with the secA2 operon. The only gene that did not contribute to ecological performance was Lr_70770, which encoded a putative adhesin. Given the large number of putative adhesins in the genome of L. reuteri 100-23 (Table 3), it is possible that redundancy exists in mechanisms that confer adherence.

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