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Open Access Research article

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

Ken-ichi Kucho1*, Takashi Yamanaka2, Hideo Sasakawa3, Samira R Mansour4 and Toshiki Uchiumi1

Author Affiliations

1 Graduate School of Science and Engineering, Kagoshima University, 1-21-35 Korimoto, Kagoshima 890-0065, Japan

2 Department of Forest Microbiology, Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan

3 Graduate School of Natural Science and Technology, Okayama University, Tsushimanaka, Okayama 700-8530, Japan

4 Botany Department, Faculty of Science, Suez Canal University, Ismailia 41522, Egypt

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BMC Genomics 2014, 15:609  doi:10.1186/1471-2164-15-609

Published: 19 July 2014

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.

Keywords:
Comparative genome hybridization; Nitrogen fixation; Pulsed-field gel electrophoresis; Symbiosis