Origin of Bacteriochlorophyll a and the Early Diversification of Photosynthesis

Cardona, Tanai

doi:10.1371/journal.pone.0151250

Cited by 19 publications

(12 citation statements)

References 33 publications

(58 reference statements)

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“…This pattern is also observed in Fig. 1 which also contained non-phototrophic representatives of the same phyla and it is consistent with previous phylogenetic (Quaiser et al 2003, Bryant et al 2012, Sousa et al 2013, Greening et al 2015, Cardona 2016a) and phylogenomic (Ciccarelli 2006, Dutilh et al 2008, Wu and Eisen 2008, Ward et al 2009, Jun et al 2010, David and Alm 2011, Rinke et al 2013, Segata et al 2013, Marin et al 2017) studies that have repeatedly confirmed the Acidobacteria as a sister clade of the Proteobacteria, or branching within the Proteobacteria as a sister clade of the deltaproteobacteria. At the same time, the nearness of the Chlorobi to Acidobacteria and Proteobacteira is also consistent with the ChlorobiBacteroidetes-Fibrobacterere supergroup bifurcating prior to the radiation of the Proteobacteria (Wu and Eisen 2008, Jun et al 2010, David and Alm 2011, Segata et al 2013, Marin et al 2017.…”

Section: Resultssupporting

confidence: 91%

“…From this perspective, our results suggest that the last common ancestor of Bacteroidetes and Chlorobi was phototrophic and that the phylum Bacteroidetes and other nonphototrophic Chlorobi evolved after losses of photosynthesis, as a mechanism of adaptation to heterotrophic or symbiotic lifestyles. Furthermore, the phylogeny of FtsH confirms the phylogenetic proximity of Acidobacteria and Proteobacteria, which is also replicated in evolutionary studies of the bacteriochlorophyll synthesis pathway (Sousa et al 2013, Cardona 2016a, showing unequivocally that the last common ancestor of Acidobacteria and Proteobacteria was also capable of phototrophy (Cardona 2015). This implies that deltaproteobacteria and non-phototrophic gamma-, beta-, and alpha-proteobacteria diversified after losses of photochemical RCs.…”

Section: Discussionsupporting

confidence: 63%

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Early emergence of the FtsH proteases involved in photosystem II repair

Shao¹,

Cardona²,

Nixon³

2018

Photosynt.

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Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair form a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of photosynthetic water oxidation chemistry.

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Section: Resultssupporting

confidence: 91%

Section: Discussionsupporting

confidence: 63%

Early emergence of the FtsH proteases involved in photosystem II repair

Shao¹,

Cardona²,

Nixon³

2018

Photosynt.

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“…PCC 6803; the membranes were solubilized using 2% dodecyl-β-maltoside and loaded on 4%–14% clear-native gel (41). Abbreviations used: PSI[ 1 ] and PSI[ 3 ], monomer and trimer of PSI, respectively; PSII[ 2 ], dimer of PSII; CpcA/B[ 6 ], approximately 100 kDa heterohexamer of CpcA and CpcB phycobilinoproteins. (B) Colored bands corresponding to PS complexes of G .…”

Section: Supporting Informationmentioning

confidence: 99%

“…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 ]. So far, 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.…”

Section: Introductionmentioning

confidence: 99%

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Unique double concentric ring organization of light harvesting complexes in Gemmatimonas phototrophica

et al. 2017

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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.

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Evolution of Photosynthesis

Cardona

2017

Encyclopedia of Life Sciences

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Photosynthesis originated once during the early Archaean due to the emergence of photochemical reaction centres, the biological nanomachines that convert the energy of light into chemical energy. The evolution of the photosynthetic machinery is consistent with a single origin of photosynthesis followed by an early diversification event that resulted in the rapid evolution of distinct reaction centre types and pigment forms. One of these reaction centres specialised in highly oxidising photochemistry, which facilitated the oxidation of Mn and the evolution of the water‐oxidising cluster of Photosystem II . In addition, the last common ancestor of all photosynthetic organisms can be traced back to a period of time near the root or at the root of the tree of life of bacteria, with the current distribution of photosynthesis being the result of widespread loss of photosynthetic capacity and horizontal gene transfer. Key Concepts Photosynthesis originated at least 3.5 billion years ago, but it could be much older. Photosynthesis evolved only once in ancestral forms of bacteria. Type I and Type II reaction centres originated from an ancestral gene duplication event. The last common ancestor of photosynthetic bacteria had type I and type II reaction centres. Photosystem II originated from the close interaction of a Type I and Type II reaction centre. The ancestral homodimeric Photosystem II was able to catalyse the oxidation of water. The last common ancestor of photosynthetic bacteria had protochlorophyllide and chlorophyllide reductase and could make pigments similar to chlorophyll a and bacteriochlorophyll g . Nitrogenase and the chlorophyll synthesis enzymes originated from an ancient gene duplication event predating the diversification of bacteria. The current distribution of photosynthesis in bacteria is explained by widespread loss of photosynthesis and horizontal gene transfer.

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Origin of Bacteriochlorophyll a and the Early Diversification of Photosynthesis

Cited by 19 publications

References 33 publications

Early emergence of the FtsH proteases involved in photosystem II repair

Early emergence of the FtsH proteases involved in photosystem II repair

Unique double concentric ring organization of light harvesting complexes in Gemmatimonas phototrophica

Evolution of Photosynthesis

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