Complex origins of chloroplast membranes with photosynthetic machineries: multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event?

AbstractThe paradigm “cyanobacterial origin of chloroplasts” is currently viewed as an established fact. However, we may have to re-consider the origin of chloroplast membranes, because membranes are not replicated by their own. It is the genes for lipid biosynthetic enzymes that are inherited. In the current understandings, these enzymes became encoded by the nuclear genome as a result of endosymbiotic gene transfer from the endosymbiont. However, we previously showed that many enzymes involved in the synthesis of chloroplast peptidoglycan and glycolipids did not originate from cyanobacteria. Here I present results of comprehensive phylogenetic analysis of chloroplast enzymes involved in fatty acid and lipid biosynthesis, as well as additional chloroplast components related to photosynthesis and gene expression. Four types of phylogenetic relationship between chloroplast enzymes (encoded by the chloroplast and nuclear genomes) and cyanobacterial counterparts were found: type 1, chloroplast enzymes diverged from inside of cyanobacterial clade; type 2, chloroplast and cyanobacterial enzymes are sister groups; type 3, chloroplast enzymes originated from homologs of bacteria other than cyanobacteria; type 4, chloroplast enzymes diverged from eukaryotic homologs. Estimation of evolutionary distances suggested that the acquisition times of chloroplast enzymes were diverse, indicating that multiple gene transfers accounted for the chloroplast enzymes analyzed. Based on the results, I try to relax the tight logic of the endosymbiotic origin of chloroplasts involving a single endosymbiotic event by proposing alternative hypotheses. The hypothesis of host-directed chloroplast formation proposes that glycolipid synthesis ability had been acquired by the eukaryotic host before the acquisition of chloroplast ribosomes. Chloroplast membrane system could have been provided by the host, whereas cyanobacteria contributed to the genes for the genetic and photosynthesis systems, at various times, either before or after the formation of chloroplast membranes. The origin(s) of chloroplasts seems to be more complicated than the single event of primary endosymbiosis.

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Protein translocons in photosynthetic organelles of Paulinella chromatophora

Acta Societatis Botanicorum Poloniae ◽

10.5586/asbp.2014.053 ◽

2014 ◽

Vol 83 (4) ◽

pp. 399-407 ◽

Cited By ~ 8

Author(s):

Przemysław Gagat ◽

Paweł Mackiewicz

Keyword(s):

Protein Import ◽

Nuclear Genome ◽

Vesicular Trafficking ◽

Plastid Gene ◽

Endosymbiotic Gene Transfer ◽

Redox Sensor ◽

Proposed Model ◽

Number Of Genes ◽

The Common ◽

Chromatophore Membrane

The rhizarian amoeba Paulinella chromatophora harbors two photosynthetic cyanobacterial endosymbionts (chromatophores), acquired independently of primary plastids of glaucophytes, red algae and green plants. These endosymbionts have lost many essential genes, and transferred substantial number of genes to the host nuclear genome via endosymbiotic gene transfer (EGT), including those involved in photosynthesis. This indicates that, similar to primary plastids, Paulinella endosymbionts must have evolved a transport system to import their EGT-derived proteins. This system involves vesicular trafficking to the outer chromatophore membrane and presumably a simplified Tic-like complex at the inner chromatophore membrane. Since both sequenced Paulinella strains have been shown to undergo differential plastid gene losses, they do not have to possess the same set of Toc and Tic homologs. We searched the genome of Paulinella FK01 strain for potential Toc and Tic homologs, and compared the results with the data obtained for Paulinella CCAC 0185 strain, and 72 cyanobacteria, eight Archaeplastida as well as some other bacteria. Our studies revealed that chromatophore genomes from both Paulinella strains encode the same set of translocons that could potentially create a simplified but fully-functional Tic-like complex at the inner chromatophore membranes. The common maintenance of the same set of translocon proteins in two Paulinella strains suggests a similar import mechanism and/or supports the proposed model of protein import. Moreover, we have discovered a new putative Tic component, Tic62, a redox sensor protein not identified in previous comparative studies of Paulinella translocons.

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The economics of endosymbiotic gene transfer and the evolution of organellar genomes

10.1101/2020.10.01.322487 ◽

2020 ◽

Cited By ~ 1

Author(s):

Steven Kelly

Keyword(s):

Gene Transfer ◽

Host Cell ◽

Protein Import ◽

Nuclear Genome ◽

Selective Advantage ◽

Endosymbiotic Gene Transfer ◽

Organellar Genomes ◽

Evolution Of Life ◽

A Cell ◽

Life On Earth

AbstractThe endosymbiosis of the bacterial progenitors of mitochondrion and the chloroplast are landmark events in the evolution of life on earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of genes found in living relatives of their ancestors. While some of the 95% of missing organellar genes have been discarded, many have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Here we demonstrate that the energy liberated or consumed by a cell as a result of endosymbiotic gene transfer can be sufficient to provide a selectable advantage for retention or nuclear-transfer of organellar genes in eukaryotic cells. We further demonstrate that for realistic estimates of protein abundances, organellar protein import costs, host cell sizes, and cellular investment in organelles that it is energetically favourable to transfer the majority of organellar genes to the nuclear genome. Moreover, we show that the selective advantage of such transfers is sufficiently large to enable such events to rapidly reach fixation. Thus, endosymbiotic gene transfer can be advantageous in the absence of any additional benefit to the host cell, providing new insight into the processes that have shaped eukaryotic genome evolution.One sentence summaryThe high copy number of organellar genomes renders endosymbiotic gene transfer energetically favourable for the vast majority of organellar genes.

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The economics of organellar gene loss and endosymbiotic gene transfer

Genome Biology ◽

10.1186/s13059-021-02567-w ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Steven Kelly

Keyword(s):

Gene Transfer ◽

Nuclear Genome ◽

Energy Budgets ◽

Net Energy ◽

Endosymbiotic Gene Transfer ◽

Organellar Genomes ◽

Chloroplast Genomes ◽

Evolution Of Life ◽

The Difference ◽

Life On Earth

Abstract Background The endosymbiosis of the bacterial progenitors of the mitochondrion and the chloroplast are landmark events in the evolution of life on Earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of the genes found in living relatives of their ancestors. While many of the 95% of missing organellar genes have been discarded, others have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Results Here, we demonstrate that the difference in the per-cell copy number of the organellar and nuclear genomes presents an energetic incentive to the cell to either delete organellar genes or transfer them to the nuclear genome. We show that, for the majority of transferred organellar genes, the energy saved by nuclear transfer exceeds the costs incurred from importing the encoded protein into the organelle where it can provide its function. Finally, we show that the net energy saved by endosymbiotic gene transfer can constitute an appreciable proportion of total cellular energy budgets and is therefore sufficient to impart a selectable advantage to the cell. Conclusion Thus, reduced cellular cost and improved energy efficiency likely played a role in the reductive evolution of mitochondrial and chloroplast genomes and the transfer of organellar genes to the nuclear genome.

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Are Cyanobacteria an Ancestor of Chloroplasts or Just One of the Gene Donors for Plants and Algae?

Genes ◽

10.3390/genes12060823 ◽

2021 ◽

Vol 12 (6) ◽

pp. 823

Author(s):

Naoki Sato

Keyword(s):

Phylogenetic Trees ◽

Expression System ◽

Phosphate Limitation ◽

Oxygenic Photosynthesis ◽

Independent Gene ◽

Essential Components ◽

Glycolipid Synthesis ◽

A Cell ◽

Chloroplast Formation ◽

Important Evidence

Chloroplasts of plants and algae are currently believed to originate from a cyanobacterial endosymbiont, mainly based on the shared proteins involved in the oxygenic photosynthesis and gene expression system. The phylogenetic relationship between the chloroplast and cyanobacterial genomes was important evidence for the notion that chloroplasts originated from cyanobacterial endosymbiosis. However, studies in the post-genomic era revealed that various substances (glycolipids, peptidoglycan, etc.) shared by cyanobacteria and chloroplasts are synthesized by different pathways or phylogenetically unrelated enzymes. Membranes and genomes are essential components of a cell (or an organelle), but the origins of these turned out to be different. Besides, phylogenetic trees of chloroplast-encoded genes suggest an alternative possibility that chloroplast genes could be acquired from at least three different lineages of cyanobacteria. We have to seriously examine that the chloroplast genome might be chimeric due to various independent gene flows from cyanobacteria. Chloroplast formation could be more complex than a single event of cyanobacterial endosymbiosis. I present the “host-directed chloroplast formation” hypothesis, in which the eukaryotic host cell that had acquired glycolipid synthesis genes as an adaptation to phosphate limitation facilitated chloroplast formation by providing glycolipid-based membranes (pre-adaptation). The origins of the membranes and the genome could be different, and the origin of the genome could be complex.

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Too rigid to fold: Carotenoid-dependent decrease in thylakoid fluidity hampers the formation of chloroplast grana

Plant Physiology ◽

10.1093/plphys/kiaa009 ◽

2020 ◽

Author(s):

Michał Bykowski ◽

Radosław Mazur ◽

Joanna Wójtowicz ◽

Szymon Suski ◽

Maciej Garstka ◽

...

Keyword(s):

Membrane System ◽

Land Plants ◽

Lipid Phase ◽

Lipid Matrix ◽

Chloroplast Membranes ◽

Dynamic Changes ◽

Ps Ii ◽

Structural Aberrations ◽

2D And 3D

Abstract In chloroplasts of land plants, the thylakoid network is organized into appressed regions called grana stacks and loosely arranged parallel stroma thylakoids. Many factors determining such intricate structural arrangements have been identified so far, including various thylakoid-embedded proteins, and polar lipids that build the thylakoid matrix. Although carotenoids are important components of proteins and the lipid phase of chloroplast membranes, their role in determining the thylakoid network structure remains elusive. We studied 2D and 3D thylakoid network organization in carotenoid-deficient mutants (ccr1-1, lut5-1, szl1-1, and szl1-1npq1-2) of Arabidopsis (Arabidopsis thaliana) to reveal the structural role of carotenoids in the formation and dynamics of the internal chloroplast membrane system. The most significant structural aberrations took place in chloroplasts of the szl1-1 and szl1-1npq1-2 plants. Increased lutein/carotene ratio in these mutants impaired the formation of grana, resulting in a significant decrease in the number of thylakoids used to build a particular stack. Further, combined biochemical and biophysical analyses revealed that hampered grana folding was related to decreased thylakoid membrane fluidity and significant changes in the amount, organization, and phosphorylation status of photosystem (PS) II (PSII) supercomplexes in the szl1-1 and szl1-1npq1-2 plants. Such changes resulted from a synergistic effect of lutein overaccumulation in the lipid matrix and a decreased level of carotenes bound with PS core complexes. Moreover, more rigid membrane in the lutein overaccumulating plants led to binding of Rubisco to the thylakoid surface, additionally providing steric hindrance for the dynamic changes in the level of membrane folding.

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A Freeze-Etch Study of Acinetobacter SP. Grown on a Hydrocarbon Substrate

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100050883 ◽

1974 ◽

Vol 32 ◽

pp. 174-175

Author(s):

C. L. Scott ◽

W. R. Finnerty

Keyword(s):

Membrane System ◽

Structural Distortion ◽

Intracytoplasmic Membrane ◽

Gram Negative ◽

Sectioned Material ◽

Acinetobacter Sp

Acinetobacter sp. HO-1-N, a gram-negative hydrocarbon oxidizing bacterium previously designated Micrococcus cerificans, has been shown to sequester the hydrocarbon into intracytoplasmic pools as a result of growth on this substrate. In hydrocarbon grown cells, an intracytoplasmic membrane system was also observed along with a doubling of cellular phospholipids (Z). However, using conventional dehydration and embedding procedures in preparing thin sectioned material, the hydrocarbon is extracted from the cells. This may lead to structural distortion, consequently, the freeze-etch technique was applied to preserve the integrity of the cell.

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Scanning Electron Microscopy of the Red Pulp of the Spleen

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s042482010006653x ◽

1971 ◽

Vol 29 ◽

pp. 496-497

Author(s):

Masayuki Miyoshi

Keyword(s):

Electron Microscope ◽

Ringer Solution ◽

Conclusive Evidence ◽

Sinus Wall ◽

Transmission Electron ◽

Type 3 ◽

Cytoplasmic Processes ◽

Splenic Red Pulp ◽

Scanning Electron ◽

Red Pulp

In spite of various attempts, conclusive evidence to explain blood passage in the splenic red pulp does not seem to have been presented. Scanning electron microscope (SEM) observations on the rabbit spleen, originally performed by us, revealed that the sinus was lined by a perforated lattice composed of longitudinally extended rod cells and transverse cytoplasmic processes, and that perforations in the lattice were continuous to the spaces among the stellate reticulum cells of the cord. In the present study the observation was extended to the dog and rat spleens, in which the cord is more developed than in the rabbit in order to clarify the possible differences in the fine structure of the sinus wall. An attempt was also made to examine the development and distribution of macrophage in the blood passage of the red pulp.Spleens were washed and fixed by perfusion with Ringer solution and then with buffered glutaraldehyde. Small tissue cubes were dehydrated with acetone, dried in air and heated with gold. Observations were made by a JEOL SEM Type-3. One air dried tissue cube was cut into small pieces and post fixed with buffered OsO4 for examination under the transmission electron microscope (TEM).

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A potassium permanganate fixative for membranes in sections

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100161175 ◽

1990 ◽

Vol 48 (3) ◽

pp. 722-723

Author(s):

Jindan Song

Keyword(s):

Potassium Permanganate ◽

Cultured Cells ◽

Calf Serum ◽

Trisodium Citrate ◽

Membrane System ◽

Adenocarcinoma Cell Line ◽

Mouse Embryo Fibroblast ◽

African Green Monkey Kidney ◽

Adenocarcinoma Cell ◽

Green Monkey

Potassium permanganate has been used as a fixative for the botanical specimen and membrane system in thin section by Glauert (1975). A new potassium permanganate fixative ( Trisodium citrate 60mM, Potassium chloride 25mM, Magnesium chloride 35mM, and Potassium permanganate 125mM ) for localizing membranous system in whole_mount cultured cells with standard trasmission electron microscopy and phase_contrast microscopy has been developed). Here, we report that using this new potassium permanganate fixative for membranous system in sections.Cultured cells, CV_1 (African green monkey kidney epithelial cells), Balb/c 3T3 ( Mouse embryo fibroblast ) and MCF_7 (Human adenocarcinoma cell line) were used for this study. All cells were grown on 35mm plastic dishes in DME medium containing 5% calf serum at 37 c with 100% humidity and 5% CO2. Using the potassium permanganate fixative to fix the cells for about 7 minutes. After fixation, the cells were dehydrated in a graded series of ethanol.

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