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. 2011:3:702-14.
doi: 10.1093/gbe/evr064. Epub 2011 Jul 6.

Reductive evolution of bacterial genome in insect gut environment

Naruo Nikoh  1 , Takahiro Hosokawa, Kenshiro Oshima, Masahira Hattori, Takema Fukatsu
Affiliations

Reductive evolution of bacterial genome in insect gut environment

Naruo Nikoh et al. Genome Biol Evol. 2011.

Abstract

Obligate endocellular symbiotic bacteria of insects and other organisms generally exhibit drastic genome reduction. Recently, it was shown that symbiotic gut bacteria of some stinkbugs also have remarkably reduced genomes. Here, we report the complete genome sequence of such a gut bacterium Ishikawaella capsulata of the plataspid stinkbug Megacopta punctatissima. Gene repertoire and evolutionary patterns, including AT richness and elevated evolutionary rate, of the 745,590 bp genome were strikingly similar to those of obligate γ-proteobacterial endocellular insect symbionts like Buchnera in aphids and Wigglesworthia in tsetse flies. Ishikawaella was suggested to supply essential amino acids for the plant-sucking stinkbug as Buchnera does for the host aphid. Although Buchnera is phylogenetically closer to Wigglesworthia than to Ishikawaella, in terms of gene repertoire Buchnera was similar to Ishikawaella rather than to Wigglesworthia, providing a possible case of genome-level convergence of gene content. Meanwhile, several notable differences were identified between the genomes of Ishikawaella and Buchnera, including retention of TCA cycle genes and lack of flagellum-related genes in Ishikawaella, which may reflect their adaptation to distinct symbiotic habitats. Unexpectedly, Ishikawaella retained fewer genes related to cell wall synthesis and lipid metabolism than many endocellular insect symbionts. The plasmid of Ishikawaella encoded genes for arginine metabolism and oxalate detoxification, suggesting the possibility of additional Ishikawaella roles similar to those of human gut bacteria. Our data highlight strikingly similar evolutionary patterns that are shared between the extracellular and endocellular insect symbiont genomes.

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Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
(A) An adult female of Megacopta punctatissima. (B) A posterior midgut dissected from an adult female. The symbiotic midgut section used for shotgun library construction is shown. (C) A transmission electron micrograph of the symbiotic midgut section, wherein symbiont cells are densely packed. Abbreviations: hg, hindgut; mep, midgut epithelium; Mpt, Malpighian tubule; and sym, symbiont cell.
F<sc>IG</sc>. 2.—
FIG. 2.—
A circular view of the Ishikawaella genome. On the GC skew circle, red and blue indicate GC-rich and poor, respectively. On the CDS circle, colors indicate functional categories as shown at the bottom.
F<sc>IG</sc>. 3.—
FIG. 3.—
Phylogenetic placement of Ishikawaella in the γ-Proteobacteria. A maximum likelihood phylogeny inferred from concatenated 50 ribosomal protein sequences (6,435 aligned amino acid sites) is shown. Statistical supports (>70%) for each clade are shown at each node in the order of maximum likelihood, Bayesian, and neighbor-joining analyses. Asterisks denote statistical support values lower than 70%.
F<sc>IG</sc>. 4.—
FIG. 4.—
Comparison of the metabolic gene repertoire between Ishikawaella, insect endocellular symbionts, and free-living γ-proteobacteria. The minimal number of genes for a metabolic pathway is shown in each of the brackets. Color indicates the ratio of retained genes to the minimal gene set for a metabolic pathway: green for 100%, orange for 99–75%, yellow for 74–50%, pink for 49–25%, and gray for 24–0%. Asterisk denotes that the bacterium possesses an alternative pathway for biosynthesis of the final product. Number in the parentheses shows the minimal number of genes for the alternative pathway.
F<sc>IG</sc>. 5.—
FIG. 5.—
An overview of the Ishikawaella metabolism and transport. The main elements of metabolic pathways and transporters that are retained and lost in the Ishikawaella genome are shown in black and red, respectively. Amino acids are in solid boxes. Vitamins and coenzymes are in dashed boxes.
F<sc>IG</sc>. 6.—
FIG. 6.—
Biosynthetic pathways of essential amino acids (A), nonessential amino acids (B), vitamins (C), and cofactors (D) retained in the Ishikawaella genome. Plasmid-encoded enzyme genes are in brackets. Parentheses indicate that their synthetic pathways encoded in the Ishikawaella genome are incomplete, whereas asterisks imply that the missing final step enzymes (strikethrough) are probably complemented by corresponding enzymes of either Ishikawaella or host insect origin (see supplementary table S5, Supplementary Material online).
F<sc>IG</sc>. 7.—
FIG. 7.—
Cluster analysis of 47 bacterial genomes, including the Ishikawaella genome, on the basis of their gene repertoire. An index reflecting gene content similarity was calculated for each of all pairs of the bacterial genomes, a distance matrix was constructed from the similarity indices, and the bacterial genomes were clustered into a tree topology under the neighbor-joining algorism. Bacterial names are shown in italic; in brackets are bacterial phyla; in parentheses are host organisms for endosymbionts. Colored bacterial names indicate red, obligate endocellular insect symbionts; blue, facultative endocellular insect symbionts/parasites; and green, obligate endocellular symbionts of non-arthropod organisms. Colored genome sizes indicate red, smaller than 1.0 Mb; blue, smaller than 1.5 Mb.
F<sc>IG</sc>. 8.—
FIG. 8.—
Estimation of the ancestral gene contents and gene losses in the evolutionary course of Ishikawaella and allied endocellular insect symbionts. The phylogenetic tree is a part of figure 3. Number above each of the branches is the number of lost OGGs since the last node. Underlined number at each of the nodes is the number of OGGs present/the expected genome size at the node. Numbers on the right side of each bacterial name indicate number of intact OGGs/number of pseudogenes/the genome size. COG categories remarkably lost and/or pseudogenized in specific branches (highlighted in supplementary table S8, Supplementary Material online) are shown.
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