Choi Jinyeong, Palanichamy Pradeep, Tanaka Hirotaka, Kondo Takumasa, Gruwell Matthew E, Husnik Filip
Evolution, Cell Biology, and Symbiosis Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa 904-0495, Japan.
Faculty of Agriculture, Ehime University, Matsuyama, Ehime 790-8566, Japan.
Mol Biol Evol. 2025 Jun 4;42(6). doi: 10.1093/molbev/msaf125.
Symbiotic microorganisms are subject to a complex interplay of environmental and population-genetic pressures that drive their gene loss. Despite the widely held perception that ancient symbionts have stable genomes, even tiny genomes experience ongoing pseudogenization. Whether these tiny genomes also experience bursts of rapid gene loss is, however, less understood. Giant scale insects (Monophlebidae) feed on plant sap and rely on the symbiotic bacterium Walczuchella, which provides them with essential nutrients. When compared with other ancient symbionts with similar genome sizes, such as Karelsulcia, Walczuchella's genome was previously reported as unusually pseudogene-rich (10% of coding sequences). However, this result was based on only one genome assembly, raising questions about the assembly quality or a recent ecological shift such as co-symbiont acquisition driving the gene loss. Here, we generated six complete genomes of Walczuchella from three genera of giant scales, each with distinct co-symbiotic partners. We show that all the genomes are highly degraded, and particularly genes related to the cellular envelope and energy metabolism seem to be undergoing pseudogenization. Apart from general mechanisms driving genome reduction, such as the long-term intracellular lifestyle with transmission bottlenecks, we hypothesize that a more profound loss of DNA replication and repair genes, together with recent co-obligate symbiont acquisitions, likely contribute to the accelerated degradation of Walczuchella genomes. Our results highlight that even ancient symbionts with small genomes can experience significant bursts of gene loss when stochastic processes erase a gene that accelerates gene loss or when the selection pressure changes such as after co-symbiont acquisition.
共生微生物受到环境和群体遗传压力的复杂相互作用影响，这些压力驱动着它们的基因丢失。尽管人们普遍认为古老的共生体具有稳定的基因组，但即使是微小的基因组也在持续经历假基因化。然而，这些微小的基因组是否也会经历快速的基因丢失爆发，却鲜为人知。大型昆虫（独角仙科）以植物汁液为食，并依赖共生细菌瓦尔楚切拉菌，该细菌为它们提供必需的营养物质。与其他基因组大小相似的古老共生体（如卡雷尔苏尔西亚菌）相比，瓦尔楚切拉菌的基因组先前被报道富含异常多的假基因（占编码序列的10%）。然而，这一结果仅基于一个基因组组装，引发了关于组装质量或近期生态转变（如共共生体获取导致基因丢失）的疑问。在这里，我们从三个大型昆虫属中生成了六个瓦尔楚切拉菌的完整基因组，每个属都有不同的共共生伙伴。我们表明，所有基因组都高度退化，特别是与细胞包膜和能量代谢相关的基因似乎正在经历假基因化。除了驱动基因组缩减的一般机制（如具有传播瓶颈的长期细胞内生活方式）外，我们推测DNA复制和修复基因的更严重丢失，以及近期共专性共生体的获取，可能导致了瓦尔楚切拉菌基因组的加速退化。我们的结果强调，即使是基因组较小的古老共生体，当随机过程抹去一个加速基因丢失或选择压力发生变化（如共共生体获取后）的基因时，也可能经历显著的基因丢失爆发。
