Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga.

McFadden, Geoffrey I.; Gilson, Paul R.; Hofmann, Chr; Adcock, Gregory J.; Maier, Uwe‐G.

doi:10.1073/pnas.91.9.3690

Cited by 143 publications

(76 citation statements)

References 17 publications

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“…Aside from P. chromatophora, there is one other photosynthetic clade among the Cercozoa: the chlorarachniophytes. These net-forming amoebae, which are only distantly related to the Euglyphida, obtained a plastid by secondary endosymbiosis of a green alga [47]. This raised the question whether the chromatophore of P. chromatophora was also product of a secondary endosymbiosis, possibly involving a glaucophyte (whose plastids contain a peptidoglycan wall and concentrically arranged thylakoid membranes with phycobilisomes) [48], or whether it arose independently of plastids.…”

Section: Chromatophores Originated Independently Of Plastidsmentioning

confidence: 99%

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Nowack

2014

Acta Soc Bot Pol

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The evolution of plastidsPrimary plastids, the photosynthetic organelles of Plantae (i.e. green algae/land plants, red algae, and glaucophytes) evolved more than 1 billion years ago (gya) through the endosymbiotic uptake of a cyanobacterium by a heterotrophic protist host [1][2][3]. Photosynthetic carbon fixation from the newly acquired plastid relieved the host from its dependency on the continuous uptake of organic carbon molecules from the environment. In addition to photosynthetic carbon fixation, plastids provide other beneficial metabolic functions to the plant/algal cell such as the assimilation of ammonia and sulfate into amino acids [4], assembly of iron-sulfur clusters [5], de novo biosynthesis of fatty acids [6], isopentenyl diphosphate (IPP) [7], and aromatic amino acids [8]; and they contribute to pathways that are distributed over several compartments, such as photorespiration and biosynthesis of pyrimidines and folates [9][10][11].Evolution of plastids was accompanied by a strong reduction of the size of the cyanobacterial genome and the transfer of thousands of cyanobacterial genes into the host nuclear genome, a process termed endosymbiotic gene transfer (EGT) [12,13]. This resulted in proteins localized to the cyanobacterium, now a full-fledged plastid, being synthesized in the cytoplasm and then imported into the plastid through a sophisticated import machinery (the TIC/ TOC complex; short for: translocon of the inner and outer chloroplast membranes) targeted by N-terminal transit peptides [14]. A multitude of solute transporters underlie the intricate metabolic crosstalk between plastid and the surrounding cell by controlling fluxes of metabolites and ions through the double membrane system that delimits the plastid [15][16][17]. Signaling pathways from and to the plastid communicate environmental cues and the metabolic and developmental status of different compartments within the plant/algal cell [18,19]. An interplay of eukaryote-and cyanobacterium-derived proteins coordinate plastid division with the host cell cycle [20].Following the establishment of primary plastids in Plantae, photosynthetic ability spread to other eukaryotic lineages through secondary endosymbioses [21,22]. In secondary endosymbioses a red or green alga served as an endosymbiont, leading to the establishment of secondary plastids in heterokontophytes (stramenopiles), cryptophytes, haptophytes, dinoflagellates, apicomplexa, chlorarachniophytes, and euglenophytes. In most cases the only remnant of the eukaryotic symbiont is one or two extra membranes that surround the secondary plastid. The nuclear genome of the * Email: e.nowack@uni-duesseldorf.deHandling Editor: Andrzej Bodył INVITED REVIEW Acta Soc Bot Pol 83(4): 387-397 DOI: 10.5586/asbp.2014.049 Received: 2014-11-16 Accepted: 2014-12-19 Published electronically: 2014 Paulinella chromatophora -rethinking the transition from endosymbiont to organelle Eva C.M. Nowack* Department of Biology, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf...

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Section: Chromatophores Originated Independently Of Plastidsmentioning

confidence: 99%

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Nowack

2014

Acta Soc Bot Pol

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“…In order to test the validity of this order we analysed all three cryptomonad genera with embedded nucleomorphs and a selection of cryptomonads without an embedded nucleomorph. In view of the presence of pyrenoidembedded nucleomorphs in Chlorarachnion (McFadden et al, 1994c) and the remote possibility that the Chlorarachnion nucleomorph might be related to that of cryptomonads (Cavalier-Smith, 1993aSitte, 1993;Cavalier-Smith et al, 1994; we also wished to determine whether an embedded nucleomorph was ancestral or secondarily derived within cryptomonads.…”

Section: Introductionmentioning

confidence: 99%

Cryptomonad nuclear and nucleomorph 18S rRNA phylogeny

Cavalier‐Smith

Couch

Thorsteinsen

et al. 1996

European Journal of Phycology

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Nuclear and nucleomorph 18S ribosomal RNA genes from six cryptomonads were amplified by the polymerase chain reaction and sequenced. Phylogenetic trees were constructed by distance, parsimony, and maximum likelihood methods for all available cryptomonad nuclear and nucleomorph 18S rRNA sequences. Nuclear and nucleomorph trees are largely congruent and clearly disprove the idea of polyphyletic origins for cryptomonad chloroplasts. Both show the leucoplast-containing Chilomonas as the sister to all photosynthetic cryptomonads. Using 11 cryptomonad nucleomorph sequences gives more convincing evidence than before that cryptomonad nucleomorphs originated from a red alga and are not specifically related to Chloraraehnion nucleomorphs. Both trees show as a clade the genera with nucleomorphs embedded in a chloroplast-envelope invagination into the pyrenoid (Storeatula, Rhinomonas, Rhodomonas). This monophyly of embedded nucleomorphs supports the recent creation of the order Pyrenomonadales for such cryptomonads. Cryptomonads ancestrally having free nucleomorphs are much more diverse. Komma and Chroomonas, with the blue accessory pigment phycocyanin, form a clade, as do Guillardia and Cryptomonas ~, both with the red pigment phycoerythrin. The nucleomorph trees strongly show the blue Chroomonas/Komma clade as sister to all red-pigmented genera, but nuclear sequences support this weakly, if at all, being sensitive to taxon sampling. Red and blue cryptomonads probably diverged early by differential pigment loss. Nuclear sequences provide no clear evidence for the nature of the host that engulfed the ancestral symbiont. Our nuclear trees using an extensive selection of outgroups, and recent evidence from chloroplast DNA, are consistent with but do not positively support the view that the closest relatives of Cryptista (i.e. Cryptophyceae plus Goniomonadea) are the Chromobiota (i.e. Haptophyta plus Heterokonta, the latter including heterokont algae--phylum Ochrophyta), and that Cryptista and Chromobiota are appropriately classified as subkingdoms of the kingdom Chromista. Maximum likelihood often groups Goniomonas with Chilomonas, suggesting that Goniomonas may have lost both nucleomorph and plastid and that the cryptist common ancestor was photosynthetic.

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“…Each chlorarachniophyte plastid is bounded by 4 smooth membranes and contains a highly reduced nucleus, referred to as the nucleomorph, of the green algal endosymbiont in the periplastidal compartment (PPC), the space between the second and third plastid membranes (25,26). The combination of these features is unique in secondary plastids, providing incentive to study plastid targeting in this algal group.…”

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confidence: 99%

Protein targeting into secondary plastids of chlorarachniophytes

Hirakawa

Nagamune²,

Ishida³

2009

Proc. Natl. Acad. Sci. U.S.A.

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Most plastid proteins are encoded by the nuclear genome, and consequently, need to be transported into plastids across multiple envelope membranes. In diverse organisms possessing secondary plastids, nuclear-encoded plastid precursor proteins (preproteins) commonly have an N-terminal extension that consists of an endoplasmic reticulum (ER)-targeting signal peptide and a transit peptide-like sequence (TPL). This bipartite targeting peptide is believed to be necessary for targeting the preproteins into the secondary plastids. Here, we newly demonstrate the function of the bipartite targeting peptides of an algal group, chlorarachniophytes, and characterize the functional domains of the TPL in the precursor of a plastid protein, ATP synthase delta subunit (AtpD), using a GFP as a reporter molecule. We show that the C-terminal portion of the TPL is important for targeting the AtpD preprotein from the ER into the chlorarachniophyte plastids, and several positively charged amino acids in the TPL are also necessary for transporting the preprotein across the 2 innermost plastid membranes. Compared with other groups with secondary plastids, the TPL functional domains of the chlorarachniophytes are unique, which might be caused by independent acquisition of their plastids.ATP synthase delta subunit ͉ secondary endosymbiosis ͉ transit peptides ͉ bipartite targeting peptide ͉ periplastidal compartment

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Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga.

Abstract: Chlorarachniophytes are amoebold algae with unusual chloroplasts. Instead

Cited by 143 publications

References 17 publications

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Cryptomonad nuclear and nucleomorph 18S rRNA phylogeny

Protein targeting into secondary plastids of chlorarachniophytes

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