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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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Distribution of genes that belong to putative genomic islands in 57 L. reuteri strains.The strains are arranged by host and MLSA lineage [20]. Red and green colors indicate presence or absence, respectively. Genes that have been identified as rodent-specific when compared to human lineage II strains by MARKFIND are indicated by asterisks (**).
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pgen-1001314-g003: Distribution of genes that belong to putative genomic islands in 57 L. reuteri strains.The strains are arranged by host and MLSA lineage [20]. Red and green colors indicate presence or absence, respectively. Genes that have been identified as rodent-specific when compared to human lineage II strains by MARKFIND are indicated by asterisks (**).

Mentions: A summary of the host-specific genes detected by MARKFIND in comparisons between rodent and human MLSA lineage II strains is presented in Table 2. Many of these genes are mobile genetic elements. In addition, almost half of the rodent-specific genes encoded hypothetical proteins with unknown function that showed a very low conservation even among rodent strains. Only 10 genes with a functional annotation other than transposition were specific to the human lineage. Most of these genes were glycosyl-transferases from the SPS2 cluster and several enzymes (histidine decarboxylase, histidyl-tRNA synthetase, dextransucrase, two lipolytic proteins). Rodent strains possessed 93 host-specific genes with assigned functions other than DNA transposition. Most of these genes fell within the putative genomic islands identified above (Figure 1). The distribution of the genes within these islands among all strains included in the CGH analysis is shown in Figure 3. The urease cluster was the only feature that was both conserved across rodent strains and absent in isolates from other hosts. All other rodent-specific clusters showed different degrees of strain-to-strain variation. Genes encoding eleven large surface proteins and the Two-Component Regulatory System (TCS) TCS2 were rare in isolates from non-rodent hosts, while the xylose cluster and the asp3 gene of the SecA2 cluster were also detectable in isolates from pigs. The two SPS clusters, though to a large degree host-specific, showed a very high variability in gene composition among rodent strains and were also detectable in strains of lineages IV (pig) and VI (poultry/human). A second regulatory system (TCS1) and the Multidrug efflux cluster (ABC) were only detectable in a small number of rodent strains.


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)

Distribution of genes that belong to putative genomic islands in 57 L. reuteri strains.The strains are arranged by host and MLSA lineage [20]. Red and green colors indicate presence or absence, respectively. Genes that have been identified as rodent-specific when compared to human lineage II strains by MARKFIND are indicated by asterisks (**).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g003: Distribution of genes that belong to putative genomic islands in 57 L. reuteri strains.The strains are arranged by host and MLSA lineage [20]. Red and green colors indicate presence or absence, respectively. Genes that have been identified as rodent-specific when compared to human lineage II strains by MARKFIND are indicated by asterisks (**).
Mentions: A summary of the host-specific genes detected by MARKFIND in comparisons between rodent and human MLSA lineage II strains is presented in Table 2. Many of these genes are mobile genetic elements. In addition, almost half of the rodent-specific genes encoded hypothetical proteins with unknown function that showed a very low conservation even among rodent strains. Only 10 genes with a functional annotation other than transposition were specific to the human lineage. Most of these genes were glycosyl-transferases from the SPS2 cluster and several enzymes (histidine decarboxylase, histidyl-tRNA synthetase, dextransucrase, two lipolytic proteins). Rodent strains possessed 93 host-specific genes with assigned functions other than DNA transposition. Most of these genes fell within the putative genomic islands identified above (Figure 1). The distribution of the genes within these islands among all strains included in the CGH analysis is shown in Figure 3. The urease cluster was the only feature that was both conserved across rodent strains and absent in isolates from other hosts. All other rodent-specific clusters showed different degrees of strain-to-strain variation. Genes encoding eleven large surface proteins and the Two-Component Regulatory System (TCS) TCS2 were rare in isolates from non-rodent hosts, while the xylose cluster and the asp3 gene of the SecA2 cluster were also detectable in isolates from pigs. The two SPS clusters, though to a large degree host-specific, showed a very high variability in gene composition among rodent strains and were also detectable in strains of lineages IV (pig) and VI (poultry/human). A second regulatory system (TCS1) and the Multidrug efflux cluster (ABC) were only detectable in a small number of rodent strains.

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