Evidence for glycoprotein transport into complex plastids

Peschke, Madeleine; Moog, Daniel; Klingl, Andreas; Maier, Uwe G.; Hempel, Franziska

doi:10.1073/pnas.1301945110

Cited by 34 publications

(25 citation statements)

References 46 publications

(67 reference statements)

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“…For in vivo localization, the expression of the GFP fusion proteins was induced with 0.9 mM NaNO 3 for 2 days, and the cells were fixed as described previously (Peschke et al ., ). The localization was analyzed with a confocal laser scanning microscope Leica TCS SP2 using an HCX PL APO 40 × /1.25 − 0.75 Oil CS objective (Leica Microsystems, Wetzlar, Germany).…”

Section: Methodsmentioning

confidence: 97%

N‐terminal lysines are essential for protein translocation via a modified ERAD system in complex plastids

Lau

Stork

Moog

et al. 2015

Molecular Microbiology

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SummaryNuclear-encoded pre-proteins being imported into complex plastids of red algal origin have to cross up to five membranes. Thereby, transport across the second outermost or periplastidal membrane (PPM) is facilitated by SELMA (symbiont-specific ERAD-like machinery), an endoplasmic reticulum-associated degradation (ERAD)-derived machinery. Core components of SELMA are enzymes involved in ubiquitination (E1 -E3), a Cdc48 ATPase complex and Derlin proteins. These components are present in all investigated organisms with four membrane-bound complex plastids of red algal origin, suggesting a ubiquitindependent translocation process of substrates mechanistically similar to the process of retrotranslocation in ERAD. Even if, according to the current model, translocation via SELMA does not end up in the classical poly-ubiquitination, transient mono-/oligo-ubiquitination of pre-proteins might be required for the mechanism of translocation. We investigated the import mechanism of SELMA and were able to show that protein transport across the PPM depends on lysines in the N-terminal but not in the C-terminal part of pre-proteins. These lysines are predicted to be targets of ubiquitination during the translocation process. As proteins lacking the Nterminal lysines get stuck in the PPM, a 'frozen intermediate' of the translocation process could be envisioned and initially characterized.

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Section: Methodsmentioning

confidence: 97%

N‐terminal lysines are essential for protein translocation via a modified ERAD system in complex plastids

Lau

Stork

Moog

et al. 2015

Molecular Microbiology

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“…Aliquots (5 l) were applied to carbon-coated copper grids and stained as previously described (24). For ultrastructural characterization, 2 l of concentrated but unfixed cells was frozen under high pressure, freeze substituted, embedded in Epon resin, ultrathin sectioned, and poststained as described previously (25). Freeze substitution was performed with acetone containing 0.2% OsO 4 , 0.25% uranyl acetate, and 5% water.…”

Section: Methodsmentioning

confidence: 99%

New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of “Candidatus Methanoplasma termitum”

Lång

Schuldes

Klingl

et al. 2015

Appl Environ Microbiol

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253

245

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The recently discovered seventh order of methanogens, the Methanomassiliicoccales (previously referred to as "Methanoplasmatales"), so far consists exclusively of obligately hydrogen-dependent methylotrophs. We sequenced the complete genome of "Candidatus Methanoplasma termitum" from a highly enriched culture obtained from the intestinal tract of termites and compared it with the previously published genomes of three other strains from the human gut, including the first isolate of the order. Like all other strains, "Ca. Methanoplasma termitum" lacks the entire pathway for CO 2 reduction to methyl coenzyme M and produces methane by hydrogen-dependent reduction of methanol or methylamines, which is consistent with additional physiological data. However, the shared absence of cytochromes and an energy-converting hydrogenase for the reoxidation of the ferredoxin produced by the soluble heterodisulfide reductase indicates that Methanomassiliicoccales employ a new mode of energy metabolism, which differs from that proposed for the obligately methylotrophic Methanosphaera stadtmanae. Instead, all strains possess a novel complex that is related to the F 420 :methanophenazine oxidoreductase (Fpo) of Methanosarcinales but lacks an F 420 -oxidizing module, resembling the apparently ferredoxin-dependent Fpo-like homolog in Methanosaeta thermophila. Since all Methanomassiliicoccales also lack the subunit E of the membrane-bound heterodisulfide reductase (HdrDE), we propose that the Fpo-like complex interacts directly with subunit D, forming an energy-converting ferredoxin:heterodisulfide oxidoreductase. The dual function of heterodisulfide in Methanomassiliicoccales, which serves both in electron bifurcation and as terminal acceptor in a membrane-associated redox process, may be a unique characteristic of the novel order. Methanogenesis is catalyzed exclusively by members of the archaeal domain. Methanogenic archaea occur only in the phylum Euryarchaeota and are phylogenetically diverse. The species described to date fall into seven orders that differ both in the biochemistry of their catabolic pathways and in their ecological niches (1, 2).Methanogens from all basal orders (Methanopyrales, Methanococcales, and Methanobacteriales) are hydrogenotrophs. They reduce CO 2 to CH 4 via the C 1 pathway, using H 2 or sometimes formate as an electron donor (1, 2). The hydrogenotrophic pathway is found also in most of the derived lineages of methanogens (Methanomicrobiales and Methanocellales) and was most probably present already in the common ancestor of the Euryarchaeota (3). Hydrogenotrophic methanogens typically lack cytochromes and conserve energy with the methyltetrahydromethanopterin (methyl-H 4 MPT):coenzyme M methyltransferase complex (Mtr), which uses the free energy of methyl transfer to establish a Na ϩ -motive force across the membrane (4). The low-potential reducing equivalents for CO 2 reduction are provided by electron bifurcation at the cytoplasmic heterodisulfide reductase complex (HdrABC) (5, 6).Members of the orde...

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“…If these proteins contain a N-linked glycosylation site they will be glycosylated. Plant and diatom plastids contain N-linked glycoproteins that are glycosylated in the ER (plants) or CER (diatoms) and glycosylation does not prevent their import into the plastid stroma (Buren et al 2011;Peschke et al 2013;Villarejo et al 2005). The activity of some plant chloroplast proteins is dependent upon N-linked glycosylation (Buren et al 2011).…”

Section: Why Did Multiple Classes Of Euglena Plastid Targeting Preseqmentioning

confidence: 99%

Protein Targeting to the Plastid of Euglena

Durnford

Schwartzbach

2017

Advances in Experimental Medicine and Biology

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The lateral transfer of photosynthesis between kingdoms through endosymbiosis is among the most spectacular examples of evolutionary innovation. Euglena, which acquired a chloroplast indirectly through an endosymbiosis with a green alga, represents such an example. As with other endosymbiont-derived plastids from eukaryotes, there are additional membranes that surround the organelle, of which Euglena has three. Thus, photosynthetic genes that were transferred from the endosymbiont to the host nucleus and whose proteins are required in the new plastid, are now faced with targeting and plastid import challenges. Early immunoelectron microscopy data suggested that the light-harvesting complexes, photosynthetic proteins in the thylakoid membrane, are post-translationally targeted to the plastid via the Golgi apparatus, an unexpected discovery at the time. Proteins targeted to the Euglena plastid have complex, bipartite presequences that direct them into the endomembrane system, through the Golgi apparatus and ultimately on to the plastid, presumably via transport vesicles. From transcriptome sequencing, dozens of plastid-targeted proteins were identified, leading to the identification of two different presequence structures. Both have an amino terminal signal peptide followed by a transit peptide for plastid import, but only one of the two classes of presequences has a third domain-the stop transfer sequence. This discovery implied two different transport mechanisms; one where the protein was fully inserted into the lumen of the ER and another where the protein remains attached to, but effectively outside, the endomembrane system. In this review, we will discuss the biochemical and bioinformatic evidence for plastid targeting, discuss the evolution of the targeting system, and ultimately provide a working model for the targeting and import of proteins into the plastid of Euglena.

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Evidence for glycoprotein transport into complex plastids

Cited by 34 publications

References 46 publications

N‐terminal lysines are essential for protein translocation via a modified ERAD system in complex plastids

N‐terminal lysines are essential for protein translocation via a modified ERAD system in complex plastids

New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of “Candidatus Methanoplasma termitum”

Protein Targeting to the Plastid of Euglena

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