光营养细菌 Gemmatimonas phototrophica 中水平转移的光合作用基因的最小转录调控。

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-09-17 Epub Date: 2024-08-27 DOI:10.1128/msystems.00706-24
Karel Kopejtka, Jürgen Tomasch, Sahana Shivaramu, Mohit Kumar Saini, David Kaftan, Michal Koblížek
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引用次数: 0

摘要

细菌门 Gemmatimonadota 的第一个光营养成员 Gemmatimonas phototrophica AP64T 通过远距离水平基因转移从一种紫色细菌获得了其所有的光合作用基因。在这里,我们研究了这些在祖先体内受氧和光严格控制的基因是如何整合到新宿主的调控系统中的。G. phototrophica 在有氧和半氧条件下生长良好,基因表达几乎没有差异。在有氧条件下,G. phototrophica 在 80 µmol photon m-2 s-1 的光照强度下生长最佳,而更高的光照强度会产生抑制作用。在最佳光照强度下,转录组对暗光转换的反应微乎其微,而在较高光照强度下(200 µmol photon m-2 s-1),基因表达的变化已经很强,但仍然是短暂的。有趣的是,在任何测试条件下,单线态氧防御都没有被激活。我们的研究结果表明,G. phototrophica 既不具有紫色细菌中已知的光合作用基因的氧依赖性抑制,也不具有需氧光养菌中描述的光依赖性抑制。相反,G. phototrophica 进化成了一种喜欢低氧浓度的低光照物种。在这些条件下,该细菌无需复杂的调控机制就能安全地进行光异养代谢:横向基因转移是细菌获得新基因的主要机制之一。然而,这仅仅是第一步,因为被转移的基因还必须在功能和调控上整合到接受者的细胞机制中。Gemmatimonas phototrophica 是细菌门 Gemmatimonadota 的一员,它的光合作用基因是通过紫色细菌的远距离水平基因转移获得的。因此,它代表了一个独特的自然实验,在这个实验中,光合作用的整套基因被移植到了一个遥远的宿主体内。我们发现 G. phototrophica 缺乏紫色细菌常见的光合作用基因表达对氧浓度和光照强度的调控。这限制了它在氧气减少的弱光环境中生长。了解横向转移基因的调控不仅对微生物进化很重要,而且对合成生物学和新型生物工程学也很重要,因为这些都依赖于外来基因的成功整合。
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Minimal transcriptional regulation of horizontally transferred photosynthesis genes in phototrophic bacterium Gemmatimonas phototrophica.

The first phototrophic member of the bacterial phylum Gemmatimonadota, Gemmatimonas phototrophica AP64T, received all its photosynthesis genes via distant horizontal gene transfer from a purple bacterium. Here, we investigated how these acquired genes, which are tightly controlled by oxygen and light in the ancestor, are integrated into the regulatory system of its new host. G. phototrophica grew well under aerobic and semiaerobic conditions, with almost no difference in gene expression. Under aerobic conditions, the growth of G. phototrophica was optimal at 80 µmol photon m-2 s-1, while higher light intensities had an inhibitory effect. The transcriptome showed only a minimal response to the dark-light shift at optimal light intensity, while the exposure to a higher light intensity (200 µmol photon m-2 s-1) induced already stronger but still transient changes in gene expression. Interestingly, a singlet oxygen defense was not activated under any conditions tested. Our results indicate that G. phototrophica possesses neither the oxygen-dependent repression of photosynthesis genes known from purple bacteria nor the light-dependent repression described in aerobic anoxygenic phototrophs. Instead, G. phototrophica has evolved as a low-light species preferring reduced oxygen concentrations. Under these conditions, the bacterium can safely employ its photoheterotrophic metabolism without the need for complex regulatory mechanisms.

Importance: Horizontal gene transfer is one of the main mechanisms by which bacteria acquire new genes. However, it represents only the first step as the transferred genes have also to be functionally and regulatory integrated into the recipient's cellular machinery. Gemmatimonas phototrophica, a member of bacterial phylum Gemmatimonadota, acquired its photosynthesis genes via distant horizontal gene transfer from a purple bacterium. Thus, it represents a unique natural experiment, in which the entire package of photosynthesis genes was transplanted into a distant host. We show that G. phototrophica lacks the regulation of photosynthesis gene expressions in response to oxygen concentration and light intensity that are common in purple bacteria. This restricts its growth to low-light habitats with reduced oxygen. Understanding the regulation of horizontally transferred genes is important not only for microbial evolution but also for synthetic biology and the engineering of novel organisms, as these rely on the successful integration of foreign genes.

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来源期刊
mSystems
mSystems Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍: mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.
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