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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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Comparison of the genomic location that contains the accessory SecA2 cluster in L. reuteri 100-23.Gene map of the accessory SecA2 cluster in Lactobacillus reuteri 100-23 and the same genomic region in strains F275 (MLSA lineage II) and CF48-3A and ATCC55730 (MLSA lineage VI). Genes are colored according to differences in GC content when compared to the genome background (39%). The PCR products shown were generated with primers that targeted conserved genes that flank the location of the SecA2 cluster (primer sites are shown by red bars).
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pgen-1001314-g006: Comparison of the genomic location that contains the accessory SecA2 cluster in L. reuteri 100-23.Gene map of the accessory SecA2 cluster in Lactobacillus reuteri 100-23 and the same genomic region in strains F275 (MLSA lineage II) and CF48-3A and ATCC55730 (MLSA lineage VI). Genes are colored according to differences in GC content when compared to the genome background (39%). The PCR products shown were generated with primers that targeted conserved genes that flank the location of the SecA2 cluster (primer sites are shown by red bars).

Mentions: The SecA2 cluster was detected by PCR in most strains from rodents and pigs (MLSA lineages I, III, IV, and V), while it is rare in isolates from human and poultry hosts (MLSA lineages II and VI). This auxiliary protein secretion system is present in a limited number of gram-positive bacteria and mycobacteria in addition to the canonical SecA system [49]. Conservation of the SecA2 cluster with other members of the Class Bacilli and sparse distribution among different species of lactobacilli implies that this system was horizontally acquired by only a few Lactobacillus lineages. LGT of this cluster in L. reuteri is supported by the presence of mobile genetic elements (Lr_70899 and Lr_70901) within the cluster, a low GC content (Figure 6), and by analysis with Alien_hunter (Figure 1). As shown in Figure S2, gene content within the accessory Sec cluster is conserved in L. gasseri, Streptococcus gordonii, and L. reuteri 100-23. In streptococci, the accessory SecA2 system facilitates the selective export of glycosylated serine-rich proteins that often function as adhesins [49], [50]. Though we do not yet know which proteins are secreted through this pathway in L. reuteri, the surface proteins Lr_70886, Lr_70902, and Lr_70903 are adjacent to the cluster in the genome of 100-23. Of those, Lr_70902 is unusually serine rich (35% serine), and the serine residues may be glycosylated by glycosyltransferases associated with the SecA2 cluster (Lr_70896–Lr_70898) analogous to serine rich surface protein in streptococci, such as GspB [49]–[51].


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)

Comparison of the genomic location that contains the accessory SecA2 cluster in L. reuteri 100-23.Gene map of the accessory SecA2 cluster in Lactobacillus reuteri 100-23 and the same genomic region in strains F275 (MLSA lineage II) and CF48-3A and ATCC55730 (MLSA lineage VI). Genes are colored according to differences in GC content when compared to the genome background (39%). The PCR products shown were generated with primers that targeted conserved genes that flank the location of the SecA2 cluster (primer sites are shown by red bars).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001314-g006: Comparison of the genomic location that contains the accessory SecA2 cluster in L. reuteri 100-23.Gene map of the accessory SecA2 cluster in Lactobacillus reuteri 100-23 and the same genomic region in strains F275 (MLSA lineage II) and CF48-3A and ATCC55730 (MLSA lineage VI). Genes are colored according to differences in GC content when compared to the genome background (39%). The PCR products shown were generated with primers that targeted conserved genes that flank the location of the SecA2 cluster (primer sites are shown by red bars).
Mentions: The SecA2 cluster was detected by PCR in most strains from rodents and pigs (MLSA lineages I, III, IV, and V), while it is rare in isolates from human and poultry hosts (MLSA lineages II and VI). This auxiliary protein secretion system is present in a limited number of gram-positive bacteria and mycobacteria in addition to the canonical SecA system [49]. Conservation of the SecA2 cluster with other members of the Class Bacilli and sparse distribution among different species of lactobacilli implies that this system was horizontally acquired by only a few Lactobacillus lineages. LGT of this cluster in L. reuteri is supported by the presence of mobile genetic elements (Lr_70899 and Lr_70901) within the cluster, a low GC content (Figure 6), and by analysis with Alien_hunter (Figure 1). As shown in Figure S2, gene content within the accessory Sec cluster is conserved in L. gasseri, Streptococcus gordonii, and L. reuteri 100-23. In streptococci, the accessory SecA2 system facilitates the selective export of glycosylated serine-rich proteins that often function as adhesins [49], [50]. Though we do not yet know which proteins are secreted through this pathway in L. reuteri, the surface proteins Lr_70886, Lr_70902, and Lr_70903 are adjacent to the cluster in the genome of 100-23. Of those, Lr_70902 is unusually serine rich (35% serine), and the serine residues may be glycosylated by glycosyltransferases associated with the SecA2 cluster (Lr_70896–Lr_70898) analogous to serine rich surface protein in streptococci, such as GspB [49]–[51].

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