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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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Confirmation of host-specific gene content by genomic comparisons and PCR.(A) A heatmap representation of BLASTN comparison of rodent-specific genes against sequenced L. reuteri genomes. Genes whose distribution throughout the species L. reuteri was determined by PCR are marked by arrows. (B) Distribution of host-specific genes throughout the phylogenetic spectrum of L. reuteri. A maximum likelihood tree of MLSA data from 116 L. reuteri strains is shown [20], and the strains for which genome sequences were included are marked by arrows. Pie charts showing the proportion of queried strains within lineages possessing the targeted genes (ureC, urease; Lr_70892, secA2, surface proteins Lr_70131, Lr_70581, Lr_70697, and pduC of the pdu-cbi-cob-hem cluster) as detected by PCR.
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pgen-1001314-g004: Confirmation of host-specific gene content by genomic comparisons and PCR.(A) A heatmap representation of BLASTN comparison of rodent-specific genes against sequenced L. reuteri genomes. Genes whose distribution throughout the species L. reuteri was determined by PCR are marked by arrows. (B) Distribution of host-specific genes throughout the phylogenetic spectrum of L. reuteri. A maximum likelihood tree of MLSA data from 116 L. reuteri strains is shown [20], and the strains for which genome sequences were included are marked by arrows. Pie charts showing the proportion of queried strains within lineages possessing the targeted genes (ureC, urease; Lr_70892, secA2, surface proteins Lr_70131, Lr_70581, Lr_70697, and pduC of the pdu-cbi-cob-hem cluster) as detected by PCR.

Mentions: As shown in Figure 4A, the genomic comparisons confirmed the findings obtained with the CGH analysis. The pdu-cbi-cob-hem cluster was detected in all human isolates (MLSA lineage II and VI) and the pig isolate ATCC 53608 (MLSA lineage IV), but it was only present in one of the three rodent strains. The urease cluster was strictly conserved among the three rodent strains and absent in all other genomes, while the surface proteins and the TCS2 cluster were to a large degree specific to rodents but more variable. The SecA2 and xylose clusters were detectable in rodent and porcine strains but completely absent in strains from lineage II and VI. The SPS and TCS1 clusters showed a much higher variability among rodent strains and several of the genes were datable in the lineage VI and IV strains, while most of the genes were absent in human lineage II strains. Consistent with CGH, the ABC transporter was specific to strain 100-23. To study the distribution of host-specific genomic features throughout the L. reuteri population, PCR was used to determine the presence of genes encoding SecA2, several surface proteins (Lr_70131, Lr_70581, Lr_70697, Lr_69916), UreC (the urease alpha subunit), and PduC (diol/glycerol dehydratase encoded by the pdu-cbi-cob-hem cluster) in 88 L. reuteri strains (Table S3). The results are shown in Figure 4B in a phylogenetic context. This analysis confirmed that several of the key genetic determinants identified by CGH are to a large degree associated with specific MLSA lineages and vertebrate hosts.


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)

Confirmation of host-specific gene content by genomic comparisons and PCR.(A) A heatmap representation of BLASTN comparison of rodent-specific genes against sequenced L. reuteri genomes. Genes whose distribution throughout the species L. reuteri was determined by PCR are marked by arrows. (B) Distribution of host-specific genes throughout the phylogenetic spectrum of L. reuteri. A maximum likelihood tree of MLSA data from 116 L. reuteri strains is shown [20], and the strains for which genome sequences were included are marked by arrows. Pie charts showing the proportion of queried strains within lineages possessing the targeted genes (ureC, urease; Lr_70892, secA2, surface proteins Lr_70131, Lr_70581, Lr_70697, and pduC of the pdu-cbi-cob-hem cluster) as detected by PCR.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g004: Confirmation of host-specific gene content by genomic comparisons and PCR.(A) A heatmap representation of BLASTN comparison of rodent-specific genes against sequenced L. reuteri genomes. Genes whose distribution throughout the species L. reuteri was determined by PCR are marked by arrows. (B) Distribution of host-specific genes throughout the phylogenetic spectrum of L. reuteri. A maximum likelihood tree of MLSA data from 116 L. reuteri strains is shown [20], and the strains for which genome sequences were included are marked by arrows. Pie charts showing the proportion of queried strains within lineages possessing the targeted genes (ureC, urease; Lr_70892, secA2, surface proteins Lr_70131, Lr_70581, Lr_70697, and pduC of the pdu-cbi-cob-hem cluster) as detected by PCR.
Mentions: As shown in Figure 4A, the genomic comparisons confirmed the findings obtained with the CGH analysis. The pdu-cbi-cob-hem cluster was detected in all human isolates (MLSA lineage II and VI) and the pig isolate ATCC 53608 (MLSA lineage IV), but it was only present in one of the three rodent strains. The urease cluster was strictly conserved among the three rodent strains and absent in all other genomes, while the surface proteins and the TCS2 cluster were to a large degree specific to rodents but more variable. The SecA2 and xylose clusters were detectable in rodent and porcine strains but completely absent in strains from lineage II and VI. The SPS and TCS1 clusters showed a much higher variability among rodent strains and several of the genes were datable in the lineage VI and IV strains, while most of the genes were absent in human lineage II strains. Consistent with CGH, the ABC transporter was specific to strain 100-23. To study the distribution of host-specific genomic features throughout the L. reuteri population, PCR was used to determine the presence of genes encoding SecA2, several surface proteins (Lr_70131, Lr_70581, Lr_70697, Lr_69916), UreC (the urease alpha subunit), and PduC (diol/glycerol dehydratase encoded by the pdu-cbi-cob-hem cluster) in 88 L. reuteri strains (Table S3). The results are shown in Figure 4B in a phylogenetic context. This analysis confirmed that several of the key genetic determinants identified by CGH are to a large degree associated with specific MLSA lineages and vertebrate hosts.

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