Department of Applied Chemistry and Life Science, Toyohashi University of Technology.
Institute for Plant Protection, National Agriculture and Food Research Organization.
Microbes Environ. 2024;39(3). doi: 10.1264/jsme2.ME24041.
The genomes of obligately host-restricted bacteria suffer from accumulating mildly deleterious mutations, resulting in marked size reductions. Psyllids (Hemiptera) are phloem sap-sucking insects with a specialized organ called the bacteriome, which typically harbors two vertically transmitted bacterial symbionts: the primary symbiont "Candidatus Carsonella ruddii" (Gammaproteobacteria) and a secondary symbiont that is phylogenetically diverse among psyllid lineages. The genomes of several Carsonella lineages were revealed to be markedly reduced (158-174 kb), AT-rich (14.0-17.9% GC), and structurally conserved with similar gene inventories devoted to synthesizing essential amino acids that are scarce in the phloem sap. However, limited genomic information is currently available on secondary symbionts. Therefore, the present study investigated the genomes of the bacteriome-associated dual symbionts, Secondary_AM (Gammaproteobacteria) and Carsonella_AM, in the mulberry psyllid Anomoneura mori (Psyllidae). The results obtained revealed that the Secondary_AM genome is as small and AT-rich (229,822 bp, 17.3% GC) as those of Carsonella lineages, including Carsonella_AM (169,120 bp, 16.2% GC), implying that Secondary_AM is an evolutionarily ancient obligate mutualist, as is Carsonella. Phylogenomic ana-lyses showed that Secondary_AM is sister to "Candidatus Psyllophila symbiotica" of Cacopsylla spp. (Psyllidae), the genomes of which were recently reported (221-237 kb, 17.3-18.6% GC). The Secondary_AM and Psyllophila genomes showed highly conserved synteny, sharing all genes for complementing the incomplete tryptophan biosynthetic pathway of Carsonella and those for synthesizing B vitamins. However, sulfur assimilation and carotenoid-synthesizing genes were only retained in Secondary_AM and Psyllophila, respectively, indicating ongoing gene silencing. Average nucleotide identity, gene ortholog similarity, genome-wide synteny, and substitution rates suggest that the Secondary_AM/Psyllophila genomes are more labile than Carsonella genomes.
专性宿主限制细菌的基因组积累了轻度有害突变，导致明显的大小减少。半翅目昆虫（Hemiptera）是吸食韧皮部汁液的昆虫，它们有一个专门的器官称为菌腔，通常含有两种垂直传播的细菌共生体：主要共生体“Candidatus Carsonella ruddii”（γ变形菌）和一个在半翅目谱系中具有多样系统发育的次要共生体。几个 Carsonella 谱系的基因组被揭示明显缩小（158-174kb），富含 AT（14.0-17.9%GC），结构保守，具有相似的基因库，专门用于合成在韧皮部汁液中稀缺的必需氨基酸。然而，目前关于次要共生体的基因组信息有限。因此，本研究调查了桑树半翅目昆虫 Anomoneura mori（半翅目）菌腔相关的双重共生体，即 Secondary_AM（γ变形菌）和 Carsonella_AM 的基因组。结果表明，Secondary_AM 基因组与 Carsonella 谱系一样小且富含 AT（229,822bp，17.3%GC），包括 Carsonella_AM（169,120bp，16.2%GC），这意味着 Secondary_AM 是一种古老的、进化上的专性共生体，就像 Carsonella 一样。系统基因组分析表明，Secondary_AM 与最近报道的 Cacopsylla spp.（半翅目）的“Candidatus Psyllophila symbiotica”是姐妹关系（221-237kb，17.3-18.6%GC）。Secondary_AM 和 Psyllophila 基因组表现出高度保守的基因排列，共享所有补充 Carsonella 不完全色氨酸生物合成途径的基因和合成 B 族维生素的基因。然而，硫同化和类胡萝卜素合成基因仅分别保留在 Secondary_AM 和 Psyllophila 中，表明基因沉默正在进行。平均核苷酸同一性、基因直系同源相似性、全基因组基因排列和取代率表明，Secondary_AM/Psyllophila 基因组比 Carsonella 基因组更不稳定。
