Limits...
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.

Show MeSH
Genome size estimated by PFGE. Sizes estimated with DraI- and PsiI-digested genomic DNAs are indicated by closed and open circles, respectively. Blue bars represent actual genome sizes of reference strains (indicated by asterisks). Black bars correspond to expected sizes of query genomes, calculated by subtracting total length of LCR segments from reference genome size.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Genome size estimated by PFGE. Sizes estimated with DraI- and PsiI-digested genomic DNAs are indicated by closed and open circles, respectively. Blue bars represent actual genome sizes of reference strains (indicated by asterisks). Black bars correspond to expected sizes of query genomes, calculated by subtracting total length of LCR segments from reference genome size.

Mentions: We estimated genome sizes of studied Frankia strains via PFGE of genomic DNA digested with DraI or PsiI. Sizes obtained using either restriction enzyme were mostly consistent (Figure 6). Results from two reference strains (ACN14a and CcI3) revealed that the estimated sizes were slightly smaller than actual genome sizes (Figure 6) for two reasons: i) small bands less than 50 kb migrated out of the gel; and ii) the relative migration rate of Frankia DNA was faster than that of yeast marker DNA (Additional file 3). Expected sizes of query genomes, based on the assumption that they lacked all LCR segments, are shown in Figure 6. Genome sizes of the four Alnus query strains after the above underestimation was taken into account were larger than expected (Figure 6), but were similar to that of the reference genome (ACN14a). Estimated genome sizes of the four Elaeagnus query strains were apparently larger than expected. Two strains (Ema2 and EU05) appeared to have genome sizes similar to the reference strain EAN1pec when underestimation was taken into account. Notably, the estimated genome size of EP01, in spite of the absence of more than 30% of genes, was much larger than that of EAN1pec (Table 2). An opposite situation was observed in Casuarina query strains. Although few genes were missing in genomes of CaE03, CaE04, and T7 (Table 2), their estimated genome sizes were significantly smaller than the reference strain CcI3. Little similarity in banding patterns was observed among or even within HSGs (Additional file 3), suggesting divergence of genome structure. As reported for the reference strains [4], genome sizes of the query strains were correlated with extent of their host ranges: Casuarina strains possessed the smallest genomes, Elaeagnus strains the largest, with Alnus strains intermediate.Figure 6


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)

Genome size estimated by PFGE. Sizes estimated with DraI- and PsiI-digested genomic DNAs are indicated by closed and open circles, respectively. Blue bars represent actual genome sizes of reference strains (indicated by asterisks). Black bars correspond to expected sizes of query genomes, calculated by subtracting total length of LCR segments from reference genome size.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Genome size estimated by PFGE. Sizes estimated with DraI- and PsiI-digested genomic DNAs are indicated by closed and open circles, respectively. Blue bars represent actual genome sizes of reference strains (indicated by asterisks). Black bars correspond to expected sizes of query genomes, calculated by subtracting total length of LCR segments from reference genome size.
Mentions: We estimated genome sizes of studied Frankia strains via PFGE of genomic DNA digested with DraI or PsiI. Sizes obtained using either restriction enzyme were mostly consistent (Figure 6). Results from two reference strains (ACN14a and CcI3) revealed that the estimated sizes were slightly smaller than actual genome sizes (Figure 6) for two reasons: i) small bands less than 50 kb migrated out of the gel; and ii) the relative migration rate of Frankia DNA was faster than that of yeast marker DNA (Additional file 3). Expected sizes of query genomes, based on the assumption that they lacked all LCR segments, are shown in Figure 6. Genome sizes of the four Alnus query strains after the above underestimation was taken into account were larger than expected (Figure 6), but were similar to that of the reference genome (ACN14a). Estimated genome sizes of the four Elaeagnus query strains were apparently larger than expected. Two strains (Ema2 and EU05) appeared to have genome sizes similar to the reference strain EAN1pec when underestimation was taken into account. Notably, the estimated genome size of EP01, in spite of the absence of more than 30% of genes, was much larger than that of EAN1pec (Table 2). An opposite situation was observed in Casuarina query strains. Although few genes were missing in genomes of CaE03, CaE04, and T7 (Table 2), their estimated genome sizes were significantly smaller than the reference strain CcI3. Little similarity in banding patterns was observed among or even within HSGs (Additional file 3), suggesting divergence of genome structure. As reported for the reference strains [4], genome sizes of the query strains were correlated with extent of their host ranges: Casuarina strains possessed the smallest genomes, Elaeagnus strains the largest, with Alnus strains intermediate.Figure 6

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