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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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The pan-genome of L. reuteri strains originating from rodents.Venn diagram showing gene distribution and overlap between the genomes of three rodent L. reuteri strains (100-23, MLC3, and lpuph1). Shown in parentheses are the numbers of genes after subtracting genes found in the genomes of L. reuteri strains originating from non-rodent hosts (F275, MM2-3, MM4-1a, CF48-3a, ATCC55730, and ATCC53608). Major functional classes represented among these genes are listed (genes without functional annotations are not shown).
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pgen-1001314-g008: The pan-genome of L. reuteri strains originating from rodents.Venn diagram showing gene distribution and overlap between the genomes of three rodent L. reuteri strains (100-23, MLC3, and lpuph1). Shown in parentheses are the numbers of genes after subtracting genes found in the genomes of L. reuteri strains originating from non-rodent hosts (F275, MM2-3, MM4-1a, CF48-3a, ATCC55730, and ATCC53608). Major functional classes represented among these genes are listed (genes without functional annotations are not shown).

Mentions: As shown in Figure 8, the three rodent strains shared around 1463 of the predicted protein coding genes. Of this core genome, only 25 genes were unique to rodent strains (Figure 8), confirming the CGH analysis in that only a small number of rodent specific genes are conserved among strains. Each strain possessed a significant proportion of genes that were absent in the other strains (528 proteins in 100-23; 235 in MLC3; and 309 in lpuph1), confirming the more variable gene pool among rodent strains. Of note, a large proportion of these genes were not found in the genomes of L. reuteri strains from non-rodent hosts (Figure 8). This rodent-specific accessory genome was comprised, apart from a large portion of mobile genetic elements, of the same functional groups as the genes identified by the CGH analysis to be rodent-specific (Figure 8 and Table S8). Thus, many of the rodent-specific surface proteins, glycosyltransferases involved in SPS synthesis, transport proteins, and regulatory proteins that are present in the genome of strain 100-23 are substituted by genes that are predicted to perform similar functions in strains MLC3 and lpuph1. The genomic comparisons revealed only one group of rodent-specific genes that were absent in the genome of 100-23 and were therefore not detected by CGH. These genes were all CRISPR-related and are likely to be involved in phage resistance.


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)

The pan-genome of L. reuteri strains originating from rodents.Venn diagram showing gene distribution and overlap between the genomes of three rodent L. reuteri strains (100-23, MLC3, and lpuph1). Shown in parentheses are the numbers of genes after subtracting genes found in the genomes of L. reuteri strains originating from non-rodent hosts (F275, MM2-3, MM4-1a, CF48-3a, ATCC55730, and ATCC53608). Major functional classes represented among these genes are listed (genes without functional annotations are not shown).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g008: The pan-genome of L. reuteri strains originating from rodents.Venn diagram showing gene distribution and overlap between the genomes of three rodent L. reuteri strains (100-23, MLC3, and lpuph1). Shown in parentheses are the numbers of genes after subtracting genes found in the genomes of L. reuteri strains originating from non-rodent hosts (F275, MM2-3, MM4-1a, CF48-3a, ATCC55730, and ATCC53608). Major functional classes represented among these genes are listed (genes without functional annotations are not shown).
Mentions: As shown in Figure 8, the three rodent strains shared around 1463 of the predicted protein coding genes. Of this core genome, only 25 genes were unique to rodent strains (Figure 8), confirming the CGH analysis in that only a small number of rodent specific genes are conserved among strains. Each strain possessed a significant proportion of genes that were absent in the other strains (528 proteins in 100-23; 235 in MLC3; and 309 in lpuph1), confirming the more variable gene pool among rodent strains. Of note, a large proportion of these genes were not found in the genomes of L. reuteri strains from non-rodent hosts (Figure 8). This rodent-specific accessory genome was comprised, apart from a large portion of mobile genetic elements, of the same functional groups as the genes identified by the CGH analysis to be rodent-specific (Figure 8 and Table S8). Thus, many of the rodent-specific surface proteins, glycosyltransferases involved in SPS synthesis, transport proteins, and regulatory proteins that are present in the genome of strain 100-23 are substituted by genes that are predicted to perform similar functions in strains MLC3 and lpuph1. The genomic comparisons revealed only one group of rodent-specific genes that were absent in the genome of 100-23 and were therefore not detected by CGH. These genes were all CRISPR-related and are likely to be involved in phage resistance.

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