<i>Paulinella</i>, a model for understanding plastid primary endosymbiosis

Gabr, Arwa; Grossman, Arthur R.; Bhattacharya, Debashish

doi:10.1111/jpy.13003

Cited by 42 publications

(33 citation statements)

References 44 publications

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“…Besides mitochondria and primary plastids that evolved via endosymbiosis >1 billion years ago, recently, a third organelle of primary endosymbiotic origin has been identified (1,2). The photosynthetically active 'chromatophore' of cercozoan amoebae of the genus Paulinella evolved around 100 million years ago from a cyanobacterium (3,4).…”

Section: Introductionmentioning

confidence: 99%

The puzzle of metabolite exchange and identification of putative octotrico peptide repeat expression regulators in the nascent photosynthetic organelles ofPaulinella chromatophora

Oberleitner

Poschmann

Macorano

et al. 2020

Preprint

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The cercozoan amoeba Paulinella chromatophora contains photosynthetic organelles - termed chromatophores - that evolved from a cyanobacterium, independently from plastids in plants and algae. Despite the more recent origin of the chromatophore, it shows tight integration into the host cell. It imports hundreds of nucleus-encoded proteins, and diverse metabolites are exchanged across the two chromatophore envelope membranes. However, the limited set of chromatophore-encoded transporters appears insufficient for supporting metabolic connectivity or protein import. Furthermore, chromatophore-localized biosynthetic pathways as well as multiprotein complexes include proteins of dual genetic origin, suggesting coordination of gene expression levels between chromatophore and nucleus. These findings imply that similar to the situation in mitochondria and plastids, nuclear factors evolved that control metabolite exchange and gene expression in the chromatophore. Here we show by mass spectrometric analyses of enriched insoluble protein fractions that, unexpectedly, nucleus-encoded transporters are not inserted into the chromatophore inner envelope membrane. Thus, despite the apparent maintenance of its barrier function, canonical metabolite transporters are missing in this membrane. Instead we identified several expanded groups of short chromatophore-targeted orphan proteins. Members of one of these groups are characterized by a single transmembrane helix, and others contain amphipathic helices. We hypothesize that these proteins are involved in modulating membrane permeability. Furthermore, we identified an expanded family of chromatophore-targeted helical repeat proteins. These proteins show similar domain architectures as known organelle-targeted octotrico peptide repeat expression regulators in algae and plants suggesting their convergent evolution as nuclear regulators of gene expression levels in the chromatophore.ImportanceThe endosymbiotic acquisition of mitochondria and plastids >1 billion years ago was central for the evolution of eukaryotic life. However, owing to their ancient origin, these organelles provide only limited insights into the initial stages of organellogenesis. The chromatophore in Paulinella evolved ~100 million years ago and thus, offers the possibility to gain valuable insights into early stages and common rules in organelle evolution. Critical to organellogenesis appears to be the establishment of nuclear control over metabolite exchange and gene expression in the endosymbiont. Here we show that the mechanism generating metabolic connectivity of the chromatophore fundamentally differs from the one for mitochondria and plastids, but likely rather resembles the poorly understood mechanism in various bacterial endosymbionts in plants and insects. Furthermore, we describe a novel class of chromatophore-targeted helical repeat proteins which evolved convergently to plastid-targeted expression regulators and are likely involved in gene expression control in the chromatophore.

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Section: Introductionmentioning

confidence: 99%

The puzzle of metabolite exchange and identification of putative octotrico peptide repeat expression regulators in the nascent photosynthetic organelles ofPaulinella chromatophora

Oberleitner

Poschmann

Macorano

et al. 2020

Preprint

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“…They actually got their green color because, as they moved to higher light environments, they evolved to no longer need the red pigment phycoerythrin, and thus they no longer reflect red light [40]. few times in evolutionary history, endosymbionts have become bona fide energy-producing organelles like mitochondria and plastids [see 7,16,17]. Once these cells become fixtures within the host cell, they undergo massive genome reduction, and many of their genes are transferred to the host nucleus in a process called endosymbiotic gene transfer (EGT).…”

Section: Horizontal Gene Transfermentioning

confidence: 99%

“…Another method, similar to exogenous uptake, is when some eukaryotic organisms (for example, some red algae; Porphyridium purpureum [14,15]) actually have plasmids of their own and can host bacterial plasmids in their nucleus where they can replicate and likely incorporate plasmid DNA into other DNA-bearing entities like organelles, the red algal nuclear DNA, or genomes of other organisms (Figure 6b(iv)). Lastly, when a cell ingests another cell but does not digest it, it can become an endosymbiont and, a few times in evolutionary history, endosymbionts have become bona fide energy-producing organelles like mitochondria and plastids [see 7,16,17]. Once these cells become fixtures within the host cell, they undergo massive genome reduction, and many of their genes are transferred to the host nucleus in a process called endosymbiotic gene transfer (EGT).…”

Section: Horizontal Gene Transfermentioning

confidence: 99%

Red Algal Extremophiles: Novel Genes and Paradigms

Etten

2020

Micros. Today

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“…This event involved a heterotrophic ancestor of Paulinella and an α‐cyanobacterial prey, with the latter evolving into a photosynthetic organelle termed the ‘chromatophore’ (Lauterborn et al ., 1895; Melkonian & Mollenhauer, 2005; Lhee et al ., 2021a). Given the incomplete and fragmented genomic evidence regarding early events in plastid evolution that is available from the Archaeplastida (Gabr et al ., 2020), there is a need for new models from nature or the application of synthetic biology approaches to understand this process (e.g. Mehta et al ., 2018).…”

Section: Introductionmentioning

confidence: 99%

Why is primary endosymbiosis so rare?

et al. 2021

Self Cite

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Endosymbiosis is a relationship between two organisms wherein one cell resides inside the other. This affiliation, when stable and beneficial for the 'host' cell, can result in massive genetic innovation with the foremost examples being the evolution of eukaryotic organelles, the mitochondria and plastids. Despite its critical evolutionary role, there is limited knowledge about how endosymbiosis is initially established and how host-endosymbiont biology is integrated. Here, we explore this issue, using as our model the rhizarian amoeba Paulinella, which represents an independent case of primary plastid origin that occurred c. 120 million yr ago. We propose the 'chassis and engine' model that provides a theoretical framework for understanding primary plastid endosymbiosis, potentially explaining why it is so rare.

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Paulinella, a model for understanding plastid primary endosymbiosis

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 42 publications

References 44 publications

The puzzle of metabolite exchange and identification of putative octotrico peptide repeat expression regulators in the nascent photosynthetic organelles ofPaulinella chromatophora

The puzzle of metabolite exchange and identification of putative octotrico peptide repeat expression regulators in the nascent photosynthetic organelles ofPaulinella chromatophora

Red Algal Extremophiles: Novel Genes and Paradigms

Why is primary endosymbiosis so rare?

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