Secrets of soil survival revealed by the genome sequence of Arthrobacter aurescens TC1

Abstract

Arthrobacter sp. strains are among the most frequently isolated, indigenous, aerobic bacterial genera found in soils. Member of the genus are metabolically and ecologically diverse and have the ability to survive in environmentally harsh conditions for extended periods of time. The genome of Arthrobacter aurescens strain TC1, which was originally isolated from soil at an atrazine spill site, is composed of a single 4,597,686 basepair (bp) circular chromosome and two circular plasmids, pTC1 and pTC2, which are 408,237 bp and 300,725 bp, respectively. Over 66% of the 4,702 open reading frames (ORFs) present in the TC1 genome could be assigned a putative function, and 13.2% (623 genes) appear to be unique to this bacterium, suggesting niche specialization. The genome of TC1 is most similar to that of Tropheryma, Leifsonia, Streptomyces, and Corynebacterium glutamicum, and analyses suggest that A. aurescens TC1 has expanded its metabolic abilities by relying on the duplication of catabolic genes and by funneling metabolic intermediates generated by plasmid-borne genes to chromosomally encoded pathways. The data presented here suggest that Arthrobacter's environmental prevalence may be due to its ability to survive under stressful conditions induced by starvation, ionizing radiation, oxygen radicals, and toxic chemicals.

Figure 1. Circular Representation of the Chromosome of A. aurescens TC1

Each concentric circle is numbered from the outermost circle to the inner most circle and represents genomic data for A. aurescens strain TC1 chromosome. The first and second circles represent the predicted coding sequences on the plus and minus strands, respectively, colored by functional role categories: salmon, amino acid biosynthesis; light blue, biosynthesis of cofactors and prosthetic groups and carriers; light green, cell envelope; red, cellular processes; brown, central intermediary metabolism; yellow, DNA metabolism; green, energy metabolism; purple, fatty acid and phospholipid metabolism; pink, protein fate and synthesis; orange, purines, pyrimidines, nucleosides, and nucleotides; blue, regulatory functions; grey, transcription; teal, transport and binding proteins; and black, hypothetical and conserved hypothetical proteins. The third circle displays the G + C skew: positive G + C skew in magenta and negative G + C skew in green. The fourth circle displays the rRNAs (red), sRNAs (blue), and tRNAs (green). The fifth circle displays repeated sequences of at least 50 bp long (at least 97% identity between two repeats); each color/tick size represents a different repeat. Prophage (blue ticks) and transposon (dark green ticks) genes are displayed on the sixth circle. The seventh circle displays the percentage of similarity (BLASTP searches) between TC1 and Arthrobacter sp. FB24 ORFs: >95%, full-sized black ticks; 85%–95%, three-quarter sized brown ticks; 75%–85%, three-quarter sized red ticks; 65%–75%, half-sized gold ticks; 55%–65%, half-sized yellow ticks. The eighth and ninth circles display the organism best match: L. xili (blue ticks), S. coelicolor (green ticks), and S. avermitilis (gold ticks) on circle 8. N. farcinica (red ticks), T. fusca (brown ticks), M. avium (cyan ticks), and C. efficiens (black ticks) on circle 9. The tenth circle shows the regions of atypical composition (χ² analysis).

Figure 2. Organization of the Region of the A. aurescens pTC1 Plasmid Containing Six Identical Direct Tandem Repeats of Approximately 16 kb in Length

For clarity, the locus tag (AAur_pTC1) was removed from the ORF numbers (for example, ORF number 0082 is AAur_pTC10082).

Figure 3. Circular Representations of the pTC1 and pTC2 Plasmids of A. aurescens TC1, and Comparative Linear Displays of Some of the Plasmid Regions Shared with the Strain TC1 Chromosome

(A and B) Each concentric circle of the circular figures is numbered from the outermost circle to the innermost circle. For each plasmid, the first and second circles represent the predicted coding sequences on the plus and minus strands, respectively, colored by functional role categories (see Figure 1). The third circle displays the G + C skew: positive G + C skew in magenta and negative G + C skew in green. The fourth circle displays the repeated sequences of at least 50 bp long (at least 97% identity between two repeats); each color/tick size represents a different repeat. Prophage (blue ticks) and transposon (dark green ticks) genes are displayed on the fifth circle. The sixth circle shows the regions of atypical composition (χ² analysis). (C–I) Comparative linear displays of some of the pTC1 and pTC2 sequences matching the TC1 chromosome. The percent of protein identity is indicated by the color of the connecting lines (legend on the right side of the figure). For clarity, the locus tags (AAur_ for the chromosome, and AAur_pTC1 and AAur_pTC2 for the pTC1 and pTC2 plasmids, respectively) were removed from the ORF numbers. For example, the chromosomal ORF number 2549 is AAur_2549, the pTC1 ORF number 0246 is AAur_pTC10246, and the pTC2 ORF number 0054 is AAur_pTC20054.

Figure 4. Comparative Linear Display Representing the Sequence Homologies between the A. aurescens pTC1 Plasmid, the Pseudomonas sp. pADP-1 Plasmid, and the A. nicotinivorans pAO1 Plasmid

Only selected regions for each of the three plasmids are shown. The percent of protein identity is indicated by the color of the connecting lines (legend on the bottom left side of the figure). For clarity, the locus tags (AAur_pTC1 for the pTC1 plasmid, AAK for the pADP-1 plasmid, and CAD for the pAO1 plasmid) were removed from the ORF numbers.

Figure 5. Maximum Likelihood Bootstrap Majority-Rule Consensus Tree for 16S rRNA Gene Sequences from 19 Strains Phylogenetically Related to A. aurescens TC1

Numbers adjacent to branch points are bootstrap percentages (n = 100 replicates). The bar represents 10% sequence divergence.