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2.4-A structure of the double-ring Gemmatimonas phototrophica photosystem.

ABSTRACT: Phototrophic Gemmatimonadetes evolved the ability to use solar energy following horizontal transfer of photosynthesis-related genes from an ancient phototrophic proteobacterium. The electron cryo-microscopy structure of the Gemmatimonas phototrophica photosystem at 2.4 Å reveals a unique, double-ring complex. Two unique membrane-extrinsic polypeptides, RC-S and RC-U, hold the central type 2 reaction center (RC) within an inner 16-subunit light-harvesting 1 (LH1) ring, which is encircled by an outer 24-subunit antenna ring (LHh) that adds light-gathering capacity. Femtosecond kinetics reveal the flow of energy within the RC-dLH complex, from the outer LHh ring to LH1 and then to the RC. This structural and functional study shows that G. phototrophica has independently evolved its own compact, robust, and highly effective architecture for harvesting and trapping solar energy.

SUBMITTER: Qian P

PROVIDER: S-EPMC8849296 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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2.4-Å structure of the double-ring <i>Gemmatimonas phototrophica</i> photosystem.

Qian Pu P Gardiner Alastair T AT Šímová Ivana I Naydenova Katerina K Croll Tristan I TI Jackson Philip J PJ Nupur Kloz Miroslav M Čubáková Petra P Kuzma Marek M Zeng Yonghui Y Castro-Hartmann Pablo P van Knippenberg Bart B Goldie Kenneth N KN Kaftan David D Hrouzek Pavel P Hájek Jan J Agirre Jon J Siebert C Alistair CA Bína David D Sader Kasim K Stahlberg Henning H Sobotka Roman R Russo Christopher J CJ Polívka Tomáš T Hunter C Neil CN Koblížek Michal M

Science advances 20220216 7

Phototrophic Gemmatimonadetes evolved the ability to use solar energy following horizontal transfer of photosynthesis-related genes from an ancient phototrophic proteobacterium. The electron cryo-microscopy structure of the <i>Gemmatimonas phototrophica</i> photosystem at 2.4 Å reveals a unique, double-ring complex. Two unique membrane-extrinsic polypeptides, RC-S and RC-U, hold the central type 2 reaction center (RC) within an inner 16-subunit light-harvesting 1 (LH1) ring, which is encircled b ...[more]

PMID: 35171663

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Project description: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.ImportanceHorizontal 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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2.4-A structure of the double-ring Gemmatimonas phototrophica photosystem.

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2.4-Å structure of the double-ring <i>Gemmatimonas phototrophica</i> photosystem.

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2.4-A structure of the double-ring Gemmatimonas phototrophica photosystem.

Publications

2.4-Å structure of the double-ring &lt;i&gt;Gemmatimonas phototrophica&lt;/i&gt; photosystem.

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OmicsDI is part of the ELIXIR infrastructure

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2.4-Å structure of the double-ring <i>Gemmatimonas phototrophica</i> photosystem.