Paulinella chromatophora

Macorano, Luis; Nowack, Eva C. M.

doi:10.1016/j.cub.2021.07.028

Cited by 7 publications

(5 citation statements)

References 8 publications

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“…but missing in studied Cyanophora species. The tsg 1 gene has also been identified in the “chromatophore” genome of the rhizarian testate amoeba Paulinella (the chromatophore is a photosynthetic organelle that evolved independent of canonical plastids; Macorano and Nowack, 2021 ).…”

Section: Resultsmentioning

confidence: 99%

Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes

Kim

Park

et al. 2022

Front. Plant Sci.

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The Raphidophyceae is an ecologically important eukaryotic lineage of primary producers and predators that inhabit marine and freshwater environments worldwide. These organisms are of great evolutionary interest because their plastids are the product of eukaryote-eukaryote endosymbiosis. To obtain deeper insight into the evolutionary history of raphidophycean plastids, we sequenced and analyzed the plastid genomes of three freshwater and three marine species. Our comparison of these genomes, together with the previously reported plastid genome of Heterosigma akashiwo, revealed unexpected variability in genome structure. Unlike the genomes of other analyzed species, the plastid genome of Gonyostomum semen was found to contain only a single rRNA operon, presumably due to the loss of genes from the inverted repeat (IR) region found in most plastid genomes. In contrast, the marine species Fibrocapsa japonica contains the largest IR region and overall plastid genome for any raphidophyte examined thus far, mainly due to the presence of four large gene-poor regions and foreign DNA. Two plastid genes, tyrC in F. japonica and He. akashiwo and serC in F. japonica, appear to have arisen via lateral gene transfer (LGT) from diatoms, and several raphidophyte open reading frames are demonstrably homologous to sequences in diatom plasmids and plastid genomes. A group II intron in the F. japonica psbB gene also appears to be derived by LGT. Our results provide important insights into the evolutionary history of raphidophyte plastid genomes via LGT from the plastids and plasmid DNAs of diatoms.

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Section: Resultsmentioning

confidence: 99%

Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes

Kim

Park

et al. 2022

Front. Plant Sci.

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“…Relative to the endosymbiotic origins of mitochondria and plastids from alphaproteobacteria and cyanobacteria respectively (61), the UCYN-A2 nitroplast of B. bigelowii appears to be at a much earlier stage of organellogenesis, similar to that seen in the chromatophore of the testate amoeba Paulinella (13,62). Phylogenomic studies suggest that the common UCYN-A ancestor was already associated with an ancestor of B. bigelowii, and had already undergone genome reduction, before the A1 and A2 lineages diverged ~90 Myr ago (63,64).…”

Section: Ucyn-a4 As a Possible Nitroplastmentioning

confidence: 99%

Targeted metagenomics reveals pangenomic diversity of the nitroplast (UCYN-A) and its algal host plastid

Kantor,

Robicheau,

Tolman

et al. 2024

Preprint

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UCYN-A (Cand. Atelocyanobacterium thalassa) has recently been recognized as a globally-distributed, early stage, nitrogen-fixing organelle (the 'nitroplast') of cyanobacterial origin present in select species of haptophyte algae (e.g., Braarudosphaera bigelowii). Although the nitroplast was recognized as the UCYN-A2 sublineage, it is yet to be confirmed in other sublineages of the algal/UCYN-A complex. We used water samples collected from Halifax Harbour (Bedford Basin, Nova Scotia, Canada) and the offshore Scotian Shelf to further our understanding of B. bigelowii and UCYN-A in the coastal Northwest Atlantic. Sequencing data revealed UCYN-A-associated haptophyte signatures and yielded near-complete metagenome-assembled genomes (MAGs) for UCYN-A1, UCYN-A4, and the plastid of the A4-associated haptophyte. Comparative genomics provided new insights into the pangenome of UCYN-A. The UCYN-A4 MAG is the first genome sequenced from this sublineage and shares ~85% identity with the UCYN-A2 nitroplast. Genes missing in the reduced genome of the nitroplast were also missing in the A4 MAG supporting its likely classification as a nitroplast as well. The UCYN-A1 MAG was found to be nearly 100% identical to the reference genome despite coming from different ocean basins. Time-series data paired with the recurrence of specific microbes in enrichment cultures gave insight into the microbes that frequently co-occur with the algal/UCYN-A complex (e.g., Pelagibacter ubique). Overall, our study expands knowledge of UCYN-A and its host across major ocean basins and investigates their co-occurring microbes in the coastal Northwest Atlantic (NWA), thereby facilitating future studies on the underpinnings of haptophyte-associated diazotrophy in the sea.

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“…Protein structure data have been deposited in World Wide Protein Data Bank ( https://www.rcsb.org/structure/8B6E ) ( 43 ). All study data are included in the article and/or supporting information .…”

Section: Data Materials and Software Availabilitymentioning

confidence: 99%

“…Despite their relatively recent origin (~100 Mya) compared to primary plastids that evolved ~1.6 billion years ago in the Archaeplastida, the chromatophores reached an astonishing level of cellular integration. Chromatophores are ~140 times larger in volume compared to their free-living relatives, and each Paulinella cell contains strictly two chromatophores of which one segregates to the daughter cell upon host cell division and duplicates shortly after ( 3 , 4 ). The functional replacement of chromatophore genes by nuclear genes resulted in metabolic pathways and multiprotein complexes of dual genetic origin in the chromatophore (e.g., photosystem I contains two nucleus-encoded subunits, PsaE and PsaK) ( 5 , 6 ).…”

mentioning

confidence: 99%

DNA-binding and protein structure of nuclear factors likely acting in genetic information processing in the Paulinella chromatophore

Macorano,

Binny,

Spiegl

et al. 2023

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

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The chromatophores in Paulinella are evolutionary-early-stage photosynthetic organelles. Biological processes in chromatophores depend on a combination of chromatophore and nucleus-encoded proteins. Interestingly, besides proteins carrying chromatophore-targeting signals, a large arsenal of short chromatophore-targeted proteins (sCTPs; <90 amino acids) without recognizable targeting signals were found in chromatophores. This situation resembles endosymbionts in plants and insects that are manipulated by host-derived antimicrobial peptides. Previously, we identified an expanded family of sCTPs of unknown function, named here “DNA-binding (DB)-sCTPs”. DB-sCTPs contain a ~45 amino acid motif that is conserved in some bacterial proteins with predicted functions in DNA processing. Here, we explored antimicrobial activity, DNA-binding capacity, and structures of three purified recombinant DB-sCTPs. All three proteins exhibited antimicrobial activity against bacteria involving membrane permeabilization, and bound to bacterial lipids in vitro. A combination of in vitro assays demonstrated binding of recombinant DB-sCTPs to chromatophore-derived genomic DNA sequences with an affinity in the low nM range. Additionally, we report the 1.2 Å crystal structure of one DB-sCTP. In silico docking studies suggest that helix α2 inserts into the DNA major grove and the exposed residues, that are highly variable between different DB-sCTPs, confer interaction with the DNA bases. Identification of photosystem II subunit CP43 as a potential interaction partner of one DB-sCTP, suggests DB-sCTPs to be involved in more complex regulatory mechanisms. We hypothesize that membrane binding of DB-sCTPs is related to their import into chromatophores. Once inside, they interact with the chromatophore genome potentially providing nuclear control over genetic information processing.

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Paulinella chromatophora

Cited by 7 publications

References 8 publications

Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes

Evolutionary Dynamics and Lateral Gene Transfer in Raphidophyceae Plastid Genomes

Targeted metagenomics reveals pangenomic diversity of the nitroplast (UCYN-A) and its algal host plastid

DNA-binding and protein structure of nuclear factors likely acting in genetic information processing in the Paulinella chromatophore

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