Insertion of Metabolite Transporters into the Endosymbiont Membrane(s) as a Prerequisite for Primary Endosymbiosis

Endosymbiosis ◽  
2013 ◽  
pp. 53-79
Author(s):  
Fabio Facchinelli ◽  
Andreas P. M. Weber
Keyword(s):  
Primary Endosymbiosis

Analysis of the Genome of Cyanophora paradoxa: An Algal Model for Understanding Primary Endosymbiosis

Endosymbiosis ◽  
2013 ◽  
pp. 135-148 ◽  
Author(s):  
Debashish Bhattacharya ◽  
Dana C. Price ◽  
Cheong Xin Chan ◽  
Jeferson Gross ◽  
Jürgen M. Steiner ◽  
...  
Keyword(s):  
Cyanophora Paradoxa ◽  
Primary Endosymbiosis

scholarly journals Metabolic connectivity as a driver of host and endosymbiont integration

2015 ◽  
Vol 112 (33) ◽  
pp. 10208-10215 ◽  
Author(s):  
Slim Karkar ◽  
Fabio Facchinelli ◽  
Dana C. Price ◽  
Andreas P. M. Weber ◽  
Debashish Bhattacharya
Keyword(s):  
Protein Localization ◽  
Oxygenic Photosynthesis ◽  
Cyanidioschyzon Merolae ◽  
Galdieria Sulphuraria ◽  
Eukaryotic Origin ◽  
Metabolic Connectivity ◽  
History Of ◽  
Phylogenetic Origin ◽  
Storage Networks ◽  
Primary Endosymbiosis

The origin of oxygenic photosynthesis in the Archaeplastida common ancestor was foundational for the evolution of multicellular life. It is very likely that the primary endosymbiosis that explains plastid origin relied initially on the establishment of a metabolic connection between the host cell and captured cyanobacterium. We posit that these connections were derived primarily from existing host-derived components. To test this idea, we used phylogenomic and network analysis to infer the phylogenetic origin and evolutionary history of 37 validated plastid innermost membrane (permeome) metabolite transporters from the model plant Arabidopsis thaliana. Our results show that 57% of these transporter genes are of eukaryotic origin and that the captured cyanobacterium made a relatively minor (albeit important) contribution to the process. We also tested the hypothesis that the bacterium-derived hexose-phosphate transporter UhpC might have been the primordial sugar transporter in the Archaeplastida ancestor. Bioinformatic and protein localization studies demonstrate that this protein in the extremophilic red algae Galdieria sulphuraria and Cyanidioschyzon merolae are plastid targeted. Given this protein is also localized in plastids in the glaucophyte alga Cyanophora paradoxa, we suggest it played a crucial role in early plastid endosymbiosis by connecting the endosymbiont and host carbon storage networks. In summary, our work significantly advances understanding of plastid integration and favors a host-centric view of endosymbiosis. Under this view, nuclear genes of either eukaryotic or bacterial (noncyanobacterial) origin provided key elements of the toolkit needed for establishing metabolic connections in the primordial Archaeplastida lineage.

scholarly journals Fatty acid photodecarboxylase is an ancient photoenzyme that forms hydrocarbons in the thylakoids of algae

2021 ◽  
Author(s):  
Solène L Y Moulin ◽  
Audrey Beyly-Adriano ◽  
Stéphan Cuiné ◽  
Stéphanie Blangy ◽  
Bertrand Légeret ◽  
...  
Keyword(s):  
Fatty Acid ◽  
Growth Conditions ◽  
Photochemical Activity ◽  
Chlorella Variabilis ◽  
Specific Subgroup ◽  
Primary Endosymbiosis ◽  
Knockout Line

Abstract Fatty acid photodecarboxylase (FAP) is one of the few enzymes that require light for their catalytic cycle (photoenzymes). FAP was first identified in the microalga Chlorella variabilis NC64A, and belongs to an algae-specific subgroup of the glucose-methanol-choline oxidoreductase family. While the FAP from C. variabilis and its Chlamydomonas reinhardtii homolog CrFAP have demonstrated in vitro activities, their activities and physiological functions have not been studied in vivo. Furthermore, the conservation of FAP activity beyond green microalgae remains hypothetical. Here, using a C. reinhardtii FAP knockout line (fap), we showed that CrFAP is responsible for the formation of 7-heptadecene, the only hydrocarbon of this alga. We further showed that CrFAP was predominantly membrane-associated and that >90% of 7-heptadecene was recovered in the thylakoid fraction. In the fap mutant, photosynthetic activity was not affected under standard growth conditions, but was reduced after cold acclimation when light intensity varied. A phylogenetic analysis that included sequences from Tara Ocean identified almost 200 putative FAPs and indicated that FAP was acquired early after primary endosymbiosis. Within Bikonta, FAP was retained in secondary photosynthetic endosymbiosis lineages but absent from those that lost the plastid. Characterization of recombinant FAPs from various algal genera (Nannochloropsis, Ectocarpus, Galdieria, Chondrus) provided experimental evidence that FAP photochemical activity was present in red and brown algae, and was not limited to unicellular species. These results thus indicate that FAP was conserved during the evolution of most algal lineages where photosynthesis was retained, and suggest that its function is linked to photosynthetic membranes.

scholarly journals Evidence supporting an antimicrobial origin of targeting peptides to endosymbiotic organelles

2020 ◽  
Author(s):  
Clotilde Garrido ◽  
Oliver D. Caspari ◽  
Yves Choquet ◽  
Francis-André Wollman ◽  
Ingrid Lafontaine
Keyword(s):  
Antimicrobial Activity ◽  
Antimicrobial Peptides ◽  
Quantitative Assessment ◽  
Chemical Properties ◽  
Signal Peptides ◽  
Fluorescent Reporter ◽  
Photosynthetic Eukaryotes ◽  
Physico Chemical ◽  
Primary Endosymbiosis ◽  
Organelle Targeting

AbstractMitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, we show that organelle targeting peptides, which are distinct from signal peptides targeting other subcellular compartments, group with a subset of antimicrobial peptides. We demonstrate that extant antimicrobial peptides target a fluorescent reporter to either the mitochondria or the chloroplast in the green alga Chlamydomonas reinhardtii and, conversely, that extant targeting peptides still display antimicrobial activity. Thus, we provide strong computational and functional evidence for an evolutionary link between organelle-targeting and antimicrobial peptides. Our results support the view that resistance of bacterial progenitors of organelles to the attack of host antimicrobial peptides has been instrumental in eukaryogenesis and in emergence of photosynthetic eukaryotes.

scholarly journals Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

2014 ◽  
Vol 83 (4) ◽  
pp. 387-397 ◽  
Author(s):  
Eva C.M. Nowack
Keyword(s):  
Carbon Fixation ◽  
Current Knowledge ◽  
Gain Control ◽  
Intermediate Stage ◽  
Photosynthetic Carbon Fixation ◽  
Photosynthetic Carbon ◽  
Encoded Proteins ◽  
Bacterial Endosymbionts ◽  
Organelle Evolution ◽  
Primary Endosymbiosis

Eukaryotes co-opted photosynthetic carbon fixation from prokaryotes by engulfing a cyanobacterium and stably integrating it as a photosynthetic organelle (plastid) in a process known as primary endosymbiosis. The sheer complexity of interactions between a plastid and the surrounding cell that started to evolve over 1 billion years ago, make it challenging to reconstruct intermediate steps in organelle evolution by studying extant plastids. Recently, the photosynthetic amoeba <em>Paulinella chromatophora</em> was identified as a much sought-after intermediate stage in the evolution of a photosynthetic organelle. This article reviews the current knowledge on this unique organism. In particular it describes how the interplay of reductive genome evolution, gene transfers, and trafficking of host-encoded proteins into the cyanobacterial endosymbiont contributed to transform the symbiont into a nascent photosynthetic organelle. Together with recent results from various other endosymbiotic associations a picture emerges that lets the targeting of host-encoded proteins into bacterial endosymbionts appear as an early step in the establishment of an endosymbiotic relationship that enables the host to gain control over the endosymbiont.

scholarly journals Paulinella , a model for understanding plastid primary endosymbiosis

2020 ◽  
Vol 56 (4) ◽  
pp. 837-843 ◽  
Author(s):  
Arwa Gabr ◽  
Arthur R. Grossman ◽  
Debashish Bhattacharya
Keyword(s):  
Primary Endosymbiosis

scholarly journals Evidence Supporting an Antimicrobial Origin of Targeting Peptides to Endosymbiotic Organelles

Cells ◽  
2020 ◽  
Vol 9 (8) ◽  
pp. 1795 ◽  
Author(s):  
Clotilde Garrido ◽  
Oliver D. Caspari ◽  
Yves Choquet ◽  
Francis-André Wollman ◽  
Ingrid Lafontaine
Keyword(s):  
Antimicrobial Activity ◽  
Antimicrobial Peptides ◽  
Quantitative Assessment ◽  
Chemical Properties ◽  
Signal Peptides ◽  
Fluorescent Reporter ◽  
Photosynthetic Eukaryotes ◽  
Physico Chemical ◽  
Primary Endosymbiosis ◽  
Organelle Targeting

Mitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, we show that organelle targeting peptides, which are distinct from signal peptides targeting other subcellular compartments, group with a subset of antimicrobial peptides. We demonstrate that extant antimicrobial peptides target a fluorescent reporter to either the mitochondria or the chloroplast in the green alga Chlamydomonas reinhardtii and, conversely, that extant targeting peptides still display antimicrobial activity. Thus, we provide strong computational and functional evidence for an evolutionary link between organelle-targeting and antimicrobial peptides. Our results support the view that resistance of bacterial progenitors of organelles to the attack of host antimicrobial peptides has been instrumental in eukaryogenesis and in the emergence of photosynthetic eukaryotes.

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