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Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum.

Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, Sachs JL, Chang JH - PLoS Pathog. (2013)

Bottom Line: We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species.This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia.Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Two diametric paradigms have been proposed to model the molecular co-evolution of microbial mutualists and their eukaryotic hosts. In one, mutualist and host exhibit an antagonistic arms race and each partner evolves rapidly to maximize their own fitness from the interaction at potential expense of the other. In the opposing model, conflicts between mutualist and host are largely resolved and the interaction is characterized by evolutionary stasis. We tested these opposing frameworks in two lineages of mutualistic rhizobia, Sinorhizobium fredii and Bradyrhizobium japonicum. To examine genes demonstrably important for host-interactions we coupled the mining of genome sequences to a comprehensive functional screen for type III effector genes, which are necessary for many Gram-negative pathogens to infect their hosts. We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species. This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia. The evolution of rhizobial type III effectors is inconsistent with the molecular arms race paradigm. Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

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Within-group genetic diversity for S. fredii, B. japonicum, is higher than the diversity within the P. syringae groups.A rooted tree was constructed from the concatenated sequences of 103 genes present in all 17 strains and Geobacter sulfurreducens PCA and Desulfovibrio vulgaris used as outgroups. The scale bar indicates the number of amino acid substitutions per site. Phylogenetic divergence (PD) was measured for each group and compared to randomly assigned groups of strains. Reliable SNPs, based on pairwise comparisons to group-specific reference strains (*), were identified and calculated per kb (see Figure S1). The percent orthology was averaged from all within-group pairwise comparisons (see Figure S2). Each group included strains with finished (underlined) and draft genome sequences.
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ppat-1003204-g001: Within-group genetic diversity for S. fredii, B. japonicum, is higher than the diversity within the P. syringae groups.A rooted tree was constructed from the concatenated sequences of 103 genes present in all 17 strains and Geobacter sulfurreducens PCA and Desulfovibrio vulgaris used as outgroups. The scale bar indicates the number of amino acid substitutions per site. Phylogenetic divergence (PD) was measured for each group and compared to randomly assigned groups of strains. Reliable SNPs, based on pairwise comparisons to group-specific reference strains (*), were identified and calculated per kb (see Figure S1). The percent orthology was averaged from all within-group pairwise comparisons (see Figure S2). Each group included strains with finished (underlined) and draft genome sequences.

Mentions: We next used multiple measures to compare the within-group diversity for the rhizobial groups to that of the group I and legume P. syringae pathovars to determine the suitability of the latter two for genomic comparisons (Figure 1; [7]). Quantitative measures of phylogenetic diversity (PD) fell within a narrow range with the two rhizobial groups having the higher PD values [29]. We also compared bacterial group PD values to those derived from equally sized groups of strains randomly assigned from the 17 used in this study. The within-group diversity of S. fredii, B. japonicum, and P. syringae, are similar, marginally, and significantly lower, respectively, relative to expectations due to chance. Additional measures based on average reliable single nucleotide polymorphisms (SNPs) per kilobase (kb) and average percent of orthologous pairs of genes were also consistent (Figures 1, S1, and S2). In total, the data demonstrate that the levels of genome-wide, within-group genetic diversity are higher in the S. fredii and B. japonicum groups, respectively, relative to either of the P. syringae groups.


Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum.

Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, Sachs JL, Chang JH - PLoS Pathog. (2013)

Within-group genetic diversity for S. fredii, B. japonicum, is higher than the diversity within the P. syringae groups.A rooted tree was constructed from the concatenated sequences of 103 genes present in all 17 strains and Geobacter sulfurreducens PCA and Desulfovibrio vulgaris used as outgroups. The scale bar indicates the number of amino acid substitutions per site. Phylogenetic divergence (PD) was measured for each group and compared to randomly assigned groups of strains. Reliable SNPs, based on pairwise comparisons to group-specific reference strains (*), were identified and calculated per kb (see Figure S1). The percent orthology was averaged from all within-group pairwise comparisons (see Figure S2). Each group included strains with finished (underlined) and draft genome sequences.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585131&req=5

ppat-1003204-g001: Within-group genetic diversity for S. fredii, B. japonicum, is higher than the diversity within the P. syringae groups.A rooted tree was constructed from the concatenated sequences of 103 genes present in all 17 strains and Geobacter sulfurreducens PCA and Desulfovibrio vulgaris used as outgroups. The scale bar indicates the number of amino acid substitutions per site. Phylogenetic divergence (PD) was measured for each group and compared to randomly assigned groups of strains. Reliable SNPs, based on pairwise comparisons to group-specific reference strains (*), were identified and calculated per kb (see Figure S1). The percent orthology was averaged from all within-group pairwise comparisons (see Figure S2). Each group included strains with finished (underlined) and draft genome sequences.
Mentions: We next used multiple measures to compare the within-group diversity for the rhizobial groups to that of the group I and legume P. syringae pathovars to determine the suitability of the latter two for genomic comparisons (Figure 1; [7]). Quantitative measures of phylogenetic diversity (PD) fell within a narrow range with the two rhizobial groups having the higher PD values [29]. We also compared bacterial group PD values to those derived from equally sized groups of strains randomly assigned from the 17 used in this study. The within-group diversity of S. fredii, B. japonicum, and P. syringae, are similar, marginally, and significantly lower, respectively, relative to expectations due to chance. Additional measures based on average reliable single nucleotide polymorphisms (SNPs) per kilobase (kb) and average percent of orthologous pairs of genes were also consistent (Figures 1, S1, and S2). In total, the data demonstrate that the levels of genome-wide, within-group genetic diversity are higher in the S. fredii and B. japonicum groups, respectively, relative to either of the P. syringae groups.

Bottom Line: We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species.This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia.Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Two diametric paradigms have been proposed to model the molecular co-evolution of microbial mutualists and their eukaryotic hosts. In one, mutualist and host exhibit an antagonistic arms race and each partner evolves rapidly to maximize their own fitness from the interaction at potential expense of the other. In the opposing model, conflicts between mutualist and host are largely resolved and the interaction is characterized by evolutionary stasis. We tested these opposing frameworks in two lineages of mutualistic rhizobia, Sinorhizobium fredii and Bradyrhizobium japonicum. To examine genes demonstrably important for host-interactions we coupled the mining of genome sequences to a comprehensive functional screen for type III effector genes, which are necessary for many Gram-negative pathogens to infect their hosts. We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species. This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia. The evolution of rhizobial type III effectors is inconsistent with the molecular arms race paradigm. Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

Show MeSH
Related in: MedlinePlus