Abstract
The majority of life on Earth depends directly or indirectly on the sun as a source of energy. The initial step of photosynthesis is facilitated by light-harvesting complexes, which capture and transfer light energy into the reaction centers (RCs). Here, we analyzed the organization of photosynthetic (PS) complexes in the bacterium G. phototrophica, which so far is the only phototrophic representative of the bacterial phylum Gemmatimonadetes. The isolated complex has a molecular weight of about 800 ± 100 kDa, which is approximately 2 times larger than the core complex of Rhodospirillum rubrum. The complex contains 62.4 ± 4.7 bacteriochlorophyll (BChl) a molecules absorbing in 2 distinct infrared absorption bands with maxima at 816 and 868 nm. Using femtosecond transient absorption spectroscopy, we determined the energy transfer time between these spectral bands as 2 ps. Single particle analyses of the purified complexes showed that they were circular structures with an outer diameter of approximately 18 nm and a thickness of 7 nm. Based on the obtained, we propose that the light-harvesting complexes in G. phototrophica form 2 concentric rings surrounding the type 2 RC. The inner ring (corresponding to the B868 absorption band) is composed of 15 subunits and is analogous to the inner light-harvesting complex 1 (LH1) in purple bacteria. The outer ring is composed of 15 more distant BChl dimers with no or slow energy transfer between them, resulting in the B816 absorption band. This completely unique and elegant organization offers good structural stability, as well as high efficiency of light harvesting. Our results reveal that while the PS apparatus of Gemmatimonadetes was acquired via horizontal gene transfer from purple bacteria, it later evolved along its own pathway, devising a new arrangement of its light harvesting complexes.
Highlights
Photosynthetic (PS) microorganisms play an important role in many of Earth’s ecosystems due to their ability to harvest light and convert it to metabolic energy [1]
Our results reveal that while the PS apparatus of Gemmatimonadetes was acquired via horizontal gene transfer from purple bacteria, it later evolved along its own pathway, devising a new arrangement of its light harvesting complexes
Based on the retention time during the size-exclusion chromatography and native gel electrophoresis, we estimated that the G. phototrophica PS complex has a molecular weight of approx. 800 ± 100 kDa (S3A Fig), which is about 2 times larger than the light-harvesting complex 1 (LH1)-reaction center (RC) core complex in R. rubrum
Summary
Photosynthetic (PS) microorganisms play an important role in many of Earth’s ecosystems due to their ability to harvest light and convert it to metabolic energy [1]. Phototrophic species were found in 7 bacterial phyla: Cyanobacteria, Proteobacteria, Chlorobi, Chloroflexi, Firmicutes, Acidobacteria, and Gemmatimonadetes [2]. The conversion of light into metabolic energy occurs in reaction centers (RCs) that carry out charge separation. Based on the terminal electron acceptor, the RCs can be divided in two groups [3]. Type 1 RCs, which use Fe-S clusters, are present in Chlorobi, Firmicutes, and Acidobacteria. Type 2 RCs, which use quinones, are possessed by Chloroflexi, Proteobacteria, and Gemmatimonadetes. Cyanobacteria are the only phototrophic prokaryotes that can evolve oxygen and possess both RC types
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