The ISME Journal ( IF 10.8 ) Pub Date : 2022-12-14 , DOI: 10.1038/s41396-022-01348-y M V Dziuba 1 , A Paulus 1, 2 , L Schramm 1 , R P Awal 1 , M Pósfai 3, 4 , C L Monteil 5 , S Fouteau 6 , R Uebe 1, 2 , D Schüler 1
Horizontal gene transfer is a powerful source of innovations in prokaryotes that can affect almost any cellular system, including microbial organelles. The formation of magnetosomes, one of the most sophisticated microbial mineral-containing organelles synthesized by magnetotactic bacteria for magnetic navigation in the environment, was also shown to be a horizontally transferrable trait. However, the mechanisms determining the fate of such genes in new hosts are not well understood, since non-adaptive gene acquisitions are typically rapidly lost and become unavailable for observation. This likely explains why gene clusters encoding magnetosome biosynthesis have never been observed in non-magnetotactic bacteria. Here, we report the first discovery of a horizontally inherited dormant gene clusters encoding biosynthesis of magnetosomes in a non-magnetotactic phototrophic bacterium Rhodovastum atsumiense. We show that these clusters were inactivated through transcriptional silencing and antisense RNA regulation, but retain functionality, as several genes were able to complement the orthologous deletions in a remotely related magnetotactic bacterium. The laboratory transfer of foreign magnetosome genes to R. atsumiense was found to endow the strain with magnetosome biosynthesis, but strong negative selection led to rapid loss of this trait upon subcultivation, highlighting the trait instability in this organism. Our results provide insight into the horizontal dissemination of gene clusters encoding complex prokaryotic organelles and illuminate the potential mechanisms of their genomic preservation in a dormant state.
中文翻译:
沉默基因簇编码非趋磁光养细菌中的磁性细胞器生物合成
水平基因转移是原核生物创新的强大来源,几乎可以影响任何细胞系统,包括微生物细胞器。磁小体的形成是趋磁细菌合成的用于在环境中进行磁导航的最复杂的微生物矿物细胞器之一,也被证明是一种水平可转移的特性。然而,决定这些基因在新宿主中命运的机制尚不清楚,因为非适应性基因获取通常会迅速丢失并且无法观察。这可能解释了为什么从未在非趋磁细菌中观察到编码磁小体生物合成的基因簇。这里,杜鹃花。我们表明这些簇通过转录沉默和反义 RNA 调节失活,但保留功能,因为几个基因能够补充远程相关趋磁细菌中的直系同源缺失。实验室将外来磁小体基因转移到R. atsumiense被发现赋予该菌株磁小体生物合成能力,但强烈的负选择导致该特性在传代培养后迅速丧失,突出了该生物体的特性不稳定性。我们的研究结果提供了对编码复杂原核细胞器的基因簇的水平传播的深入了解,并阐明了它们在休眠状态下基因组保存的潜在机制。