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, 6 (9), e24882

Biological Consequences of Ancient Gene Acquisition and Duplication in the Large Genome of Candidatus Solibacter Usitatus Ellin6076

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Biological Consequences of Ancient Gene Acquisition and Duplication in the Large Genome of Candidatus Solibacter Usitatus Ellin6076

Jean F Challacombe et al. PLoS One.

Abstract

Members of the bacterial phylum Acidobacteria are widespread in soils and sediments worldwide, and are abundant in many soils. Acidobacteria are challenging to culture in vitro, and many basic features of their biology and functional roles in the soil have not been determined. Candidatus Solibacter usitatus strain Ellin6076 has a 9.9 Mb genome that is approximately 2-5 times as large as the other sequenced Acidobacteria genomes. Bacterial genome sizes typically range from 0.5 to 10 Mb and are influenced by gene duplication, horizontal gene transfer, gene loss and other evolutionary processes. Our comparative genome analyses indicate that the Ellin6076 large genome has arisen by horizontal gene transfer via ancient bacteriophage and/or plasmid-mediated transduction, and widespread small-scale gene duplications, resulting in an increased number of paralogs. Low amino acid sequence identities among functional group members, and lack of conserved gene order and orientation in regions containing similar groups of paralogs, suggest that most of the paralogs are not the result of recent duplication events. The genome sizes of additional cultured Acidobacteria strains were estimated using pulsed-field gel electrophoresis to determine the prevalence of the large genome trait within the phylum. Members of subdivision 3 had larger genomes than those of subdivision 1, but none were as large as the Ellin6076 genome. The large genome of Ellin6076 may not be typical of the phylum, and encodes traits that could provide a selective metabolic, defensive and regulatory advantage in the soil environment.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Circular map of the Ellin6076 (Panel A) and Ellin345 (Panel B) genomes obtained from the IMG system (http://img.doe.gov).
From outside to the center: Circles 1 and 2: forward and reverse strand genes colored by COG categories; Circles 3 and 4: RNA genes (tRNAs green, sRNAs red, other RNAs black); Circles 5 and 6: mobile elements; Circle 7: GC content; Circle 8: GC skew. Colors representing the COG category codes and function definitions: cyan, [A] RNA processing and modification; light lime, [B] Chromatin structure and dynamics; light aqua, [C] Energy production and conversion; pale lavender, [D] Cell cycle control, cell division, chromosome partitioning; light crimson, [E] Amino acid transport and metabolism; light blue green, [F] Nucleotide transport and metabolism; dark pink, [G] Carbohydrate transport and metabolism; teal, [H] Coenzyme transport and metabolism; violet blue, [I] Lipid transport and metabolism; violet, [J] Translation, ribosomal structure and biogenesis; light olive, [K] Transcription; yellow, [L] Replication, recombination and repair; light brown, [M] Cell wall/membrane/envelope biogenesis; light pink, [N] Cell motility; light green, [O] Posttranslational modification, protein turnover, chaperones; orange, [P] Inorganic ion transport and metabolism; lime, [Q] Secondary metabolites biosynthesis, transport and catabolism; purple, [R] General function prediction only; aqua, [S] Function unknown; brown, [T] Signal transduction mechanisms; light blue, [U] Intracellular trafficking, secretion and vesicular transport; baby blue, [V] Defense mechanisms; lavender, [W] Extracellular structures; light red, [Y] Nuclear structure; lime green, [Z] Cytoskeleton.
Figure 2
Figure 2. Maximum-likelihood tree of the Acidobacteria subdivisions 1 and 3 (indicated to the right of the group) based on the16S rRNA gene using sequences obtained from cultivated representatives and environmental clones.
Geothrix fermentans, Holophaga foetida and Acanthopleuribacter pedi of subdivision 8 were used as an outgroup (not shown). Strains for which the genome size has been determined are highlighted in bold typeface. Internal nodes support by a bootstrap value of >95% are indicated with a filled circle and >70% with an open circle. The scale bar indicates 0.10 changes per nucleotide.

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