Possibly the most abundant group of anoxygenic phototrophs are marine photoheterotrophic Gammaproteobacteria belonging to the NOR5/OM60 clade. As little is known about their photosynthetic apparatus, the photosynthetic complexes from the marine phototrophic bacterium Congregibacter litoralis KT71 were purified and spectroscopically characterised. The intra-cytoplasmic membranes contain a smaller amount of photosynthetic complexes when compared with anaerobic purple bacteria. Moreover, the intra-cytoplasmic membranes contain only a minimum amount of peripheral LH2 complexes. The complexes are populated by bacteriochlorophyll a, spirilloxanthin and two novel ketocarotenoids, with biophysical and biochemical properties similar to previously characterised complexes from purple bacteria. The organization of the RC-LH1 complex has been further characterised using cryo-electron microscopy. The overall organisation is similar to the complex from the gammaproteobacterium Thermochromatium tepidum, with the type-II reaction centre surrounded by a slightly elliptical LH1 antenna ring composed of 16 αβ-subunits with no discernible gap or pore. The RC-LH1 and LH2 apoproteins are phylogenetically related to other halophilic species but LH2 also to some alphaproteobacterial species. It seems that the reduction of light-harvesting apparatus and acquisition of novel ketocarotenoids in Congregibacter litoralis KT71 represent specific adaptations for operating the anoxygenic photosynthesis under aerobic conditions at sea.
- Klíčová slova
- AAP, Congregibacter, Light-harvesting, Photoheterotrophy, Photosynthesis, Purple bacteria,
- MeSH
- elektronová kryomikroskopie MeSH
- fotosyntetické reakční centrum - proteinové komplexy * MeSH
- fotosyntéza MeSH
- Gammaproteobacteria * chemie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fotosyntetické reakční centrum - proteinové komplexy * MeSH
The bacterium Gemmatimonas phototrophica AP64 isolated from a freshwater lake in the western Gobi Desert represents the first phototrophic member of the bacterial phylum Gemmatimonadota. This strain was originally cultured on agar plates because it did not grow in liquid medium. In contrast, the closely related species G. groenlandica TET16 grows both on solid and in liquid media. Here, we show that the growth of G. phototrophica in liquid medium can be induced by supplementing the medium with 20 mg CaCl2 L-1. When grown at a lower concentration of calcium (2 mg CaCl2 L-1) in the liquid medium, the growth was significantly delayed, cells were elongated and lacked flagella. The elevated requirement for calcium is relatively specific as it can be partially substituted by strontium, but not by magnesium. The transcriptome analysis documented that several groups of genes involved in flagella biosynthesis and transport of transition metals were co-activated after amendment of 20 mg CaCl2 L-1 to the medium. The presented results document that G. phototrophica requires a higher concentration of calcium for its metabolism and growth compared to other Gemmatimonas species.
- Klíčová slova
- Gemmatimonas phototrophica, anoxygenic phototrophic bacteria, calcium, horizontal gene transfer, transcriptomics,
- Publikační typ
- časopisecké články MeSH
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.
- Publikační typ
- časopisecké články MeSH
Gemmatimonas phototrophica AP64 is the first phototrophic representative of the bacterial phylum Gemmatimonadetes. The cells contain photosynthetic complexes with bacteriochlorophyll a as the main light-harvesting pigment and an unknown carotenoid with a single broad absorption band at 490 nm in methanol. The carotenoid was extracted from isolated photosynthetic complexes, and purified by liquid chromatography. A combination of nuclear magnetic resonance (1H NMR, COSY, 1H-13C HSQC, 1H-13C HMBC, J-resolved, and ROESY), high-resolution mass spectroscopy, Fourier-transformed infra-red, and Raman spectroscopy was used to determine its chemical structure. The novel linear carotenoid, that we have named gemmatoxanthin, contains 11 conjugated double bonds and is further substituted by methoxy, carboxyl and aldehyde groups. Its IUPAC-IUBMB semi-systematic name is 1'-Methoxy-19'-oxo-3',4'-didehydro-7,8,1',2'-tetrahydro- Ψ, Ψ carotene-16-oic acid. To our best knowledge, the presence of the carboxyl, methoxy and aldehyde groups on a linear C40 carotenoid backbone is reported here for the first time.
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Gemmatimonas phototrophica is, so far, the only described phototrophic species of the bacterial phylum Gemmatimonadetes. Its cells contain a unique type of photosynthetic complex with the reaction center surrounded by a double ring antenna, however they can also grow in the dark using organic carbon substrates. Its photosynthesis genes were received via horizontal gene transfer from Proteobacteria. This raises two questions; how the horizontally transferred photosynthesis apparatus has integrated into the cellular machinery, and how much light-derived energy actually contributes to the cellular metabolism? To address these points, the photosynthetic reactions were studied on several levels, from photophysics of the reaction center to cellular growth. Flash photolysis measurements and bacteriochlorophyll fluorescence kinetic measurements documented the presence of fully functional type-2 reaction centers with a large light harvesting antenna. When illuminated, the bacterial cells reduced their respiration rate by 58 ± 5%, revealing that oxidative phosphorylation was replaced by photophosphorylation. Moreover, illumination also more than doubled the assimilation rates of glucose, a sugar that is mostly used for respiration. Finally, light increased the growth rates of Gemmatimonas phototrophica colonies on agar plates. All the presented data provide evidence that photosynthetic complexes are fully integrated into cellular metabolism of Gemmatimonas phototrophica, and are able to provide a substantial amount of energy for its metabolism and growth.
- Klíčová slova
- Anoxygenic phototrophs, Gemmatimonadetes, Gemmatimonadota, Photoheterotrophy, Photophosphorylation,
- MeSH
- Bacteria chemie metabolismus MeSH
- bakteriální proteiny chemie metabolismus MeSH
- bakteriochlorofyly chemie MeSH
- fluorescenční spektrometrie MeSH
- fosforylace MeSH
- fotolýza MeSH
- fotosyntetické reakční centrum - proteinové komplexy chemie MeSH
- fotosyntéza MeSH
- kinetika MeSH
- oxidace-redukce MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
- bakteriochlorofyly MeSH
- fotosyntetické reakční centrum - proteinové komplexy MeSH
The bacterial phylum Gemmatimonadetes contains members capable of performing bacteriochlorophyll-based phototrophy (chlorophototrophy). However, only one strain of chlorophototrophic Gemmatimonadetes bacteria (CGB) has been isolated to date, hampering our further understanding of their photoheterotrophic lifestyle and the evolution of phototrophy in CGB. By combining a culturomics strategy with a rapid screening technique for chlorophototrophs, we report the isolation of a new member of CGB, Gemmatimonas (G.) groenlandica sp. nov., from the surface water of a stream in the Zackenberg Valley in High Arctic Greenland. Distinct from the microaerophilic G. phototrophica strain AP64T, G. groenlandica strain TET16T is a strictly aerobic anoxygenic phototroph, lacking many oxygen-independent enzymes while possessing an expanded arsenal for coping with oxidative stresses. Its pigment composition and infra-red absorption properties are also different from G. phototrophica, indicating that it possesses a different photosystem apparatus. The complete genome sequence of G. groenlandica reveals unique and conserved features in the photosynthesis gene clusters of CGB. We further analyzed metagenome-assembled genomes of CGB obtained from soil and glacier metagenomes from Northeast Greenland, revealing a wide distribution pattern of CGB beyond the stream water investigated.
- Klíčová slova
- Gemmatimonadetes, MALDI-TOF MS, bacterial isolation, oligotrophic environment, phototrophy,
- Publikační typ
- časopisecké články MeSH