Genome-wide effects of selenium and translational uncoupling on transcription in the termite gut symbiont Treponema primita

When prokaryotic cells acquire mutations, encounter translation-inhibiting substances, or experience adverse environmental conditions that limit their ability to synthesize proteins, transcription can become uncoupled from translation. Such uncoupling is known to suppress transcription of protein-encoding genes in bacteria. Here we show that the trace element selenium controls transcription of the gene for the selenocysteine-utilizing enzyme formate dehydrogenase (fdhFSec) through a translation-coupled mechanism in the termite gut symbiont Treponema primitia, a member of the bacterial phylum Spirochaetes. We also evaluated changes in genome-wide transcriptional patterns caused by selenium limitation and by generally uncoupling translation from transcription via antibiotic-mediated inhibition of protein synthesis. We observed that inhibiting protein synthesis in T. primitia influences transcriptional patterns in unexpected ways. In addition to suppressing transcription of certain genes, the expected consequence of inhibiting protein synthesis, we found numerous examples in which transcription of genes and operons is truncated far downstream from putative promoters, is unchanged, or is even stimulated overall. These results indicate that gene regulation in bacteria allows for specific post-initiation transcriptional responses during periods of limited protein synthesis, which may depend both on translational coupling and on unclassified intrinsic elements of protein-encoding genes.

当原核细胞发生突变、接触翻译抑制物质，或遭遇限制其蛋白质合成能力的不利环境条件时，转录与翻译过程可能发生解偶联。已知这种解偶联会抑制细菌中蛋白质编码基因的转录。本研究发现，微量元素硒可通过翻译偶联机制，调控白蚁肠道共生菌普氏密螺旋体（Treponema primitia，隶属于螺旋体门（Spirochaetes））中利用硒半胱氨酸的甲酸脱氢酶编码基因（fdhFSec）的转录。我们还评估了硒限制以及通过抗生素介导的蛋白质合成抑制实现的翻译-转录普遍解偶联所引发的全基因组转录模式变化。研究发现，抑制普氏密螺旋体的蛋白质合成会以意想不到的方式改变其转录模式：除了抑制特定基因转录（这是抑制蛋白质合成的预期结果）之外，我们还发现诸多案例，基因与操纵子的转录在推定启动子下游极远处发生截断、转录水平保持不变，甚至整体上被激活。上述结果表明，细菌的基因调控机制可在蛋白质合成受限期间产生特定的转录起始后应答，这类应答可能同时依赖翻译偶联机制，以及蛋白质编码基因中尚未被分类的内在元件。