Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids.
Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids.
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DOI：
10.1093/molbev/mss180
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发表时间：
2012-12-01
影响因子：
10.7
通讯作者：
Moran, Nancy A
中科院分区：
文献类型：
--
作者：
Sloan, Daniel B;Moran, Nancy A
专性胞内细菌的基因组减少是分子进化领域中最完善的模式之一。在极端情况下，许多以汁液为食的昆虫携带着营养共生体，这些共生体的基因组如此之少，以至于我们不清楚它们是如何执行基本细胞功能的。例如，木虱（Carsonella）的主要共生体保持着迄今为止发现的最小和最富at的细菌基因组之一，并且令人惊讶地失去了许多被认为对其向宿主提供氨基酸至关重要的基因。然而，我们对这种基因组减少的极端情况的理解是有限的，因为Carsonella的基因组数据仅来自单一宿主物种，而且对木虱中“次级”细菌共生体的功能作用知之甚少。为了解决这些局限性，我们分析了木虱科（Ctenarytaina， Heteropsylla和Pachypsylla）三个不同属的对同源宿主的完整Carsonella基因组，以及其中两个宿主物种（Ctenarytaina eucalyptus和Heteropsylla cubana）的完整次级共生体基因组。尽管Carsonella的基因组在大小、结构和GC含量上通常是保守的，并且表现出全基因组的纯化选择特征，但我们发现，自宿主物种分化以来，基因丢失一直保持活跃，并对确定Carsonella共生作用的氨基酸生物合成途径产生特别大的影响。在某些情况下，额外细菌共生体的存在可能补偿卡索菌中的基因损失，因为功能基因含量表明共存共生体之间具有高度的代谢互补性。次生共生体的基因组也显示出作为垂直传播的细胞内细菌的长期进化特征，包括比通常在兼性共生体中观察到的更广泛的基因组减少。因此，与次级细菌共生体的共同进化历史可以部分解释卡索菌正在进行的基因组减少。然而，在其他寄主谱系中缺乏这些次生共生体表明，这种关系是动态的，其他机制，如寄主饮食的变化或与寄主基因组的功能协调，也必须发挥作用。
Genome reduction in obligately intracellular bacteria is one of the most well-established patterns in the field of molecular evolution. In the extreme, many sap-feeding insects harbor nutritional symbionts with genomes that are so reduced that it is not clear how they perform basic cellular functions. For example, the primary symbiont of psyllids (Carsonella) maintains one of the smallest and most AT-rich bacterial genomes ever identified and has surprisingly lost many genes that are thought to be essential for its role in provisioning its host with amino acids. However, our understanding of this extreme case of genome reduction is limited, as genomic data for Carsonella are available from only a single host species, and little is known about the functional role of "secondary" bacterial symbionts in psyllids. To address these limitations, we analyzed complete Carsonella genomes from pairs of congeneric hosts in three divergent genera within the Psyllidae (Ctenarytaina, Heteropsylla, and Pachypsylla) as well as complete secondary symbiont genomes from two of these host species (Ctenarytaina eucalypti and Heteropsylla cubana). Although the Carsonella genomes are generally conserved in size, structure, and GC content and exhibit genome-wide signatures of purifying selection, we found that gene loss has remained active since the divergence of the host species and had a particularly large impact on the amino acid biosynthesis pathways that define the symbiotic role of Carsonella. In some cases, the presence of additional bacterial symbionts may compensate for gene loss in Carsonella, as functional gene content indicates a high degree of metabolic complementarity between co-occurring symbionts. The genomes of the secondary symbionts also show signatures of long-term evolution as vertically transmitted, intracellular bacteria, including more extensive genome reduction than typically observed in facultative symbionts. Therefore, a history of co-evolution with secondary bacterial symbionts can partially explain the ongoing genome reduction in Carsonella. However, the absence of these secondary symbionts in other host lineages indicates that the relationships are dynamic and that other mechanisms, such as changes in host diet or functional coordination with the host genome, must also be at play.