Carvalho Ana S P, Wingert Sinah T, Kirsch Roy, Vogel Heiko, Kölsch Gregor, Kaltenpoth Martin
Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Hans-Knöll-Str. 8, 07745, Jena, Germany.
Evolutionary Ecology, Institute for Organismic and Molecular Evolution (iomE), Johannes Gutenberg University, Hanns-Dieter-Hüsch-Weg 15, 55128, Mainz, Germany.
EMBO Rep. 2025 Aug 8. doi: 10.1038/s44319-025-00525-2.
Symbiotic bacteria in long-term host associations frequently undergo extreme genome reduction. While they retain genes beneficial to the host, their repertoire of transcription factors is severely reduced. Here, we assessed whether genome-eroded symbionts can still regulate gene expression by characterizing the transcriptional responses of obligate symbionts in reed beetles to different temperatures and host life stages. These symbionts feature a small genome (~0.5 Mb), encoding for 9-10 essential amino acid biosynthesis pathways, 0-2 pectinases, and 4-5 transcription factors. We found that the symbionts respond to winter conditions by upregulating a heat-shock sigma factor and downregulating translation machinery. Across life stages, symbionts adjusted gene expression to meet the hosts' nutritional demands, upregulating amino acid biosynthesis in larvae, while expression and activity of host and symbiont enzymes involved in plant cell wall breakdown increased in the folivorous adults. In addition, the regulation of symbiont cell morphology genes corresponded to cell shape differences across life stages. Thus, reed beetle symbionts may use their few transcription factors to respond to the host's environment, highlighting the regulatory potential of long-term coevolved symbionts despite severely reduced genomes.
在与宿主的长期共生关系中，共生细菌常常经历极端的基因组缩减。尽管它们保留了对宿主有益的基因，但其转录因子库却大幅减少。在此，我们通过表征芦苇甲虫专性共生菌对不同温度和宿主生命阶段的转录反应，评估了基因组缩减的共生菌是否仍能调控基因表达。这些共生菌具有较小的基因组（约0.5兆碱基对），编码9至10种必需氨基酸生物合成途径、0至2种果胶酶以及4至5种转录因子。我们发现，共生菌通过上调一种热休克σ因子并下调翻译机制来应对冬季条件。在不同生命阶段，共生菌会调整基因表达以满足宿主的营养需求，在幼虫阶段上调氨基酸生物合成，而在以叶为食的成虫阶段，参与植物细胞壁分解的宿主和共生菌酶的表达及活性均增加。此外，共生菌细胞形态基因的调控与不同生命阶段的细胞形状差异相对应。因此，芦苇甲虫共生菌可能利用其为数不多的转录因子来应对宿主环境，这凸显了尽管基因组大幅缩减，但长期协同进化的共生菌仍具有调控潜力。
