Department of General Systems Studies, Graduate School of Arts and Sciences, the University of Tokyo, Meguro-ku, Tokyo, Japan.
Mol Biol Evol. 2013 Nov;30(11):2494-508. doi: 10.1093/molbev/mst153. Epub 2013 Sep 11.
Although many α- and some β-proteobacterial species are symbiotic with legumes, the evolutionary origin of nitrogen-fixing nodulation remains unclear. We examined α- and β-proteobacteria whose genomes were sequenced using large-scale phylogenetic profiling and revealed the evolutionary origin of two nodulation genes. These genes, nodI and nodJ (nodIJ), play key roles in the secretion of Nod factors, which are recognized by legumes during nodulation. We found that only the nodulating β-proteobacteria, including the novel strains isolated in this study, possess both nodIJ and their paralogous genes (DRA-ATPase/permease genes). Contrary to the widely accepted scenario of the α-proteobacterial origin of rhizobia, our exhaustive phylogenetic analysis showed that the entire nodIJ clade is included in the clade of Burkholderiaceae DRA-ATPase/permease genes, that is, the nodIJ genes originated from gene duplication in a lineage of the β-proteobacterial family. After duplication, the evolutionary rates of nodIJ were significantly accelerated relative to those of homologous genes, which is consistent with their novel function in nodulation. The likelihood analyses suggest that this accelerated evolution is not associated with changes in either nonsynonymous/synonymous substitution rates or transition/transversion rates, but rather, in the GC content. Although the low GC content of the nodulation genes has been assumed to reflect past horizontal transfer events from donor rhizobial genomes with low GC content, no rhizobial genome with such low GC content has yet been found. Our results encourage a reconsideration of the origin of nodulation and suggest new perspectives on the role of the GC content of bacterial genes in functional adaptation.
虽然许多α-和一些β-变形菌与豆科植物共生，但固氮结瘤的进化起源仍不清楚。我们使用大规模系统发育分析研究了α-和β-变形菌，揭示了两个结瘤基因的进化起源。这些基因，nodI 和 nodJ（nodIJ），在 Nod 因子的分泌中起关键作用，Nod 因子在结瘤过程中被豆科植物识别。我们发现，只有固氮β-变形菌，包括本研究中分离的新菌株，同时拥有 nodIJ 及其同源基因（DRA-ATPase/permease 基因）。与普遍接受的根瘤菌α-变形菌起源的观点相反，我们详尽的系统发育分析表明，整个 nodIJ 分支包含在伯克霍尔德氏菌科 DRA-ATPase/permease 基因分支中，即 nodIJ 基因起源于β-变形菌家族的一个谱系中的基因复制。复制后，nodIJ 的进化速度相对于同源基因明显加快，这与其在结瘤中的新功能一致。似然分析表明，这种加速进化与非同义/同义取代率或转换/颠换率的变化无关，而是与 GC 含量有关。尽管结瘤基因的低 GC 含量被认为反映了来自 GC 含量低的供体根瘤菌基因组的水平转移事件，但尚未发现 GC 含量如此低的根瘤菌基因组。我们的结果鼓励重新考虑结瘤的起源，并为细菌基因 GC 含量在功能适应中的作用提供新的视角。
