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. 2006 Jun;4(6):e188.
doi: 10.1371/journal.pbio.0040188.

V体育ios版 - Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters

Dongying Wu  1 , Sean C Daugherty, Susan E Van Aken, Grace H Pai, Kisha L Watkins, Hoda Khouri, Luke J Tallon, Jennifer M Zaborsky, Helen E Dunbar, Phat L Tran, Nancy A Moran, Jonathan A Eisen
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Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters

Dongying Wu et al. PLoS Biol. 2006 Jun.

Abstract

Mutualistic intracellular symbiosis between bacteria and insects is a widespread phenomenon that has contributed to the global success of insects. The symbionts, by provisioning nutrients lacking from diets, allow various insects to occupy or dominate ecological niches that might otherwise be unavailable. One such insect is the glassy-winged sharpshooter (Homalodisca coagulata), which feeds on xylem fluid, a diet exceptionally poor in organic nutrients. Phylogenetic studies based on rRNA have shown two types of bacterial symbionts to be coevolving with sharpshooters: the gamma-proteobacterium Baumannia cicadellinicola and the Bacteroidetes species Sulcia muelleri. We report here the sequencing and analysis of the 686,192-base pair genome of B. cicadellinicola and approximately 150 kilobase pairs of the small genome of S VSports手机版. muelleri, both isolated from H. coagulata. Our study, which to our knowledge is the first genomic analysis of an obligate symbiosis involving multiple partners, suggests striking complementarity in the biosynthetic capabilities of the two symbionts: B. cicadellinicola devotes a substantial portion of its genome to the biosynthesis of vitamins and cofactors required by animals and lacks most amino acid biosynthetic pathways, whereas S. muelleri apparently produces most or all of the essential amino acids needed by its host. This finding, along with other results of our genome analysis, suggests the existence of metabolic codependency among the two unrelated endosymbionts and their insect host. This dual symbiosis provides a model case for studying correlated genome evolution and genome reduction involving multiple organisms in an intimate, obligate mutualistic relationship. In addition, our analysis provides insight for the first time into the differences in symbionts between insects (e. g. , aphids) that feed on phloem versus those like H. coagulata that feed on xylem. Finally, the genomes of these two symbionts provide potential targets for controlling plant pathogens such as Xylella fastidiosa, a major agroeconomic problem, for which H. coagulata and other sharpshooters serve as vectors of transmission. .

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Figures

Figure 1
Figure 1. Circular View of the Baumannia Genome
Circles correspond to the following features, starting with the outermost circle: (1) forward strand genes, (2) reverse strand genes, (3) χ 2 deviation of local nucleotide composition from the genome average, (4) GC skew, (5) tRNAs (green lines), (6) rRNAs (blue lines); and (7) small RNAs (red lines). Color legend for CDSs and number of genes in each category are at the bottom.
Figure 2
Figure 2. Genome-Based Phylogenetic Analysis of Baumannia
(A) Maximum-likelihood tree of gamma-proteobacterial endosymbionts. The tree was built from concatenated alignments of 45 ribosomal proteins using the PHYML program. The bootstrap value is based upon 1,000 replications. (B) Gene order comparison of Baumannia and Blochmannia floridanus. The plot shows the locations of homologous proteins between the two genomes.
Figure 3
Figure 3. Correlation between Genomic G + C Content and the Average pI of the Proteins of Endosymbiotic and Free-Living Gammaproteobacteria
Species shown are Buchnera aphidicola APS (Ba APS), Buchnera aphidicola BP (Ba Bp), Buchnera aphidicola SG (Ba Sg), Baumannia (Bc), Blochmannia floridanus (Bf), Blochmannia pennsylvanicus (Bp), E. coli K12 (Ec), Wigglesworthia glossindia (Wg), and Yersinia pestis KIM (Yp).
Figure 4
Figure 4. Predicted Metabolic Pathways in Baumannia and the Predicted Amino Acid Biosynthesis Pathways Encoded by the Partial Genome Sequence of Sulcia
Genes that are present are in red and the corresponding catalytic pathways are illustrated in solid black lines; the genes that are absent in the Baumannia genome and genes that have not been identified in the partial Sulcia genome are in gray, and the corresponding metabolic steps are illustrated in gray lines.
Figure 5
Figure 5. Maximum-Likelihood Tree of Sulcia with Species in the Bacteroides and Chlorobi Phyla for which Complete Genomes Are Available
The tree was build using the PHYML program from the concatenated alignments of 34 ribosomal proteins. The bootstrap values are based upon 1,000 replications.
Figure 6
Figure 6. The Distribution into Functional Role Categories of the 166 Predicted Genes Encoded in the 146,384-bp Partial Sequence of the Sulcia Genome
Data are shown for all ORFs that encode proteins longer than 45 amino acids that have BLASTP matches with an E-value less than 10 −3 to proteins in complete genomes. Different fragments of the same gene are counted as one gene in the chart.
Figure 7
Figure 7. Baumannia and Sulcia Coinhabit the Bacteriomes of the Host Insects
Fluorescent in situ hybridizations were performed using oligonucleotide probes designed to hybridize selectively to the ribosomal RNA of Baumannia (green) and of Sulcia (red), respectively. Bacteriomes were obtained from Homalodisca literata (a very close relative of H. coagulata).
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References

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