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Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia.

Kucho K, Yamanaka T, Sasakawa H, Mansour SR, Uchiumi T - BMC Genomics (2014)

Bottom Line: Elaeagnus query strains were missing the greatest number (22-32%) of genes compared with the corresponding reference genome; Casuarina query strains lacked the fewest (0-4%), with Alnus query strains intermediate (14-18%).In addition, our results suggest that different dynamics of shuffling of genome content have contributed to these symbiotic and biogeographic adaptations.Conversely, rather than acquiring new genes, Casuarina strains have discarded genes to reduce genome size, suggesting an evolutionary orientation towards existence as specialist symbionts.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Science and Engineering, Kagoshima University, 1-21-35 Korimoto, Kagoshima 890-0065, Japan. kkucho@sci.kagoshima-u.ac.jp.

ABSTRACT

Background: Frankia is a genus of soil actinobacteria forming nitrogen-fixing root-nodule symbiotic relationships with non-leguminous woody plant species, collectively called actinorhizals, from eight dicotyledonous families. Frankia strains are classified into four host-specificity groups (HSGs), each of which exhibits a distinct host range. Genome sizes of representative strains of Alnus, Casuarina, and Elaeagnus HSGs are highly diverged and are positively correlated with the size of their host ranges.

Results: The content and size of 12 Frankia genomes were investigated by in silico comparative genome hybridization and pulsed-field gel electrophoresis, respectively. Data were collected from four query strains of each HSG and compared with those of reference strains possessing completely sequenced genomes. The degree of difference in genome content between query and reference strains varied depending on HSG. Elaeagnus query strains were missing the greatest number (22-32%) of genes compared with the corresponding reference genome; Casuarina query strains lacked the fewest (0-4%), with Alnus query strains intermediate (14-18%). In spite of the remarkable gene loss, genome sizes of Alnus and Elaeagnus query strains were larger than would be expected based on total length of the absent genes. In contrast, Casuarina query strains had smaller genomes than expected.

Conclusions: The positive correlation between genome size and host range held true across all investigated strains, supporting the hypothesis that size and genome content differences are responsible for observed diversity in host plants and host plant biogeography among Frankia strains. In addition, our results suggest that different dynamics of shuffling of genome content have contributed to these symbiotic and biogeographic adaptations. Elaeagnus strains, and to a lesser extent Alnus strains, have gained and lost many genes to adapt to a wide range of environments and host plants. Conversely, rather than acquiring new genes, Casuarina strains have discarded genes to reduce genome size, suggesting an evolutionary orientation towards existence as specialist symbionts.

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Venn diagram representing overlap of LCR genes amongFrankiastrains belonging to (a) Alnus, (b) Casuarina, and (c) Elaeagnus HSGs. The total number of nonredundant LCR genes is shown above the diagram. Numbers in the diagram are percentages of the nonredundant LCR genes associated with the indicated overlapping strains.
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Fig4: Venn diagram representing overlap of LCR genes amongFrankiastrains belonging to (a) Alnus, (b) Casuarina, and (c) Elaeagnus HSGs. The total number of nonredundant LCR genes is shown above the diagram. Numbers in the diagram are percentages of the nonredundant LCR genes associated with the indicated overlapping strains.

Mentions: In genomes of ACN14a, CcI3, and EAN1pec, respectively, 1,633, 185, and 2,685 genes were scored as LCR genes for at least one of the four query strains (nonredundant LCR genes; Figure 4). In Alnus and Elaeagnus HSGs, about 40% of nonredundant LCR genes were scored as LCR genes for all four query strains (Figure 4), indicating that they were commonly absent in genomes of these strains. The remaining genes were scored as LCR genes for one to three strains; the distribution of these genes was apparently unbiased, except that LCR genes specific to Asi1 and those shared with EP01 and EUr01 predominated. In the Casuarina HSG, 99% of nonredundant LCR genes were missing only in strain Ceq1; only a few or no LCR genes were associated with the other strains.Table 2


Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia.

Kucho K, Yamanaka T, Sasakawa H, Mansour SR, Uchiumi T - BMC Genomics (2014)

Venn diagram representing overlap of LCR genes amongFrankiastrains belonging to (a) Alnus, (b) Casuarina, and (c) Elaeagnus HSGs. The total number of nonredundant LCR genes is shown above the diagram. Numbers in the diagram are percentages of the nonredundant LCR genes associated with the indicated overlapping strains.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4117964&req=5

Fig4: Venn diagram representing overlap of LCR genes amongFrankiastrains belonging to (a) Alnus, (b) Casuarina, and (c) Elaeagnus HSGs. The total number of nonredundant LCR genes is shown above the diagram. Numbers in the diagram are percentages of the nonredundant LCR genes associated with the indicated overlapping strains.
Mentions: In genomes of ACN14a, CcI3, and EAN1pec, respectively, 1,633, 185, and 2,685 genes were scored as LCR genes for at least one of the four query strains (nonredundant LCR genes; Figure 4). In Alnus and Elaeagnus HSGs, about 40% of nonredundant LCR genes were scored as LCR genes for all four query strains (Figure 4), indicating that they were commonly absent in genomes of these strains. The remaining genes were scored as LCR genes for one to three strains; the distribution of these genes was apparently unbiased, except that LCR genes specific to Asi1 and those shared with EP01 and EUr01 predominated. In the Casuarina HSG, 99% of nonredundant LCR genes were missing only in strain Ceq1; only a few or no LCR genes were associated with the other strains.Table 2

Bottom Line: Elaeagnus query strains were missing the greatest number (22-32%) of genes compared with the corresponding reference genome; Casuarina query strains lacked the fewest (0-4%), with Alnus query strains intermediate (14-18%).In addition, our results suggest that different dynamics of shuffling of genome content have contributed to these symbiotic and biogeographic adaptations.Conversely, rather than acquiring new genes, Casuarina strains have discarded genes to reduce genome size, suggesting an evolutionary orientation towards existence as specialist symbionts.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Science and Engineering, Kagoshima University, 1-21-35 Korimoto, Kagoshima 890-0065, Japan. kkucho@sci.kagoshima-u.ac.jp.

ABSTRACT

Background: Frankia is a genus of soil actinobacteria forming nitrogen-fixing root-nodule symbiotic relationships with non-leguminous woody plant species, collectively called actinorhizals, from eight dicotyledonous families. Frankia strains are classified into four host-specificity groups (HSGs), each of which exhibits a distinct host range. Genome sizes of representative strains of Alnus, Casuarina, and Elaeagnus HSGs are highly diverged and are positively correlated with the size of their host ranges.

Results: The content and size of 12 Frankia genomes were investigated by in silico comparative genome hybridization and pulsed-field gel electrophoresis, respectively. Data were collected from four query strains of each HSG and compared with those of reference strains possessing completely sequenced genomes. The degree of difference in genome content between query and reference strains varied depending on HSG. Elaeagnus query strains were missing the greatest number (22-32%) of genes compared with the corresponding reference genome; Casuarina query strains lacked the fewest (0-4%), with Alnus query strains intermediate (14-18%). In spite of the remarkable gene loss, genome sizes of Alnus and Elaeagnus query strains were larger than would be expected based on total length of the absent genes. In contrast, Casuarina query strains had smaller genomes than expected.

Conclusions: The positive correlation between genome size and host range held true across all investigated strains, supporting the hypothesis that size and genome content differences are responsible for observed diversity in host plants and host plant biogeography among Frankia strains. In addition, our results suggest that different dynamics of shuffling of genome content have contributed to these symbiotic and biogeographic adaptations. Elaeagnus strains, and to a lesser extent Alnus strains, have gained and lost many genes to adapt to a wide range of environments and host plants. Conversely, rather than acquiring new genes, Casuarina strains have discarded genes to reduce genome size, suggesting an evolutionary orientation towards existence as specialist symbionts.

Show MeSH