An inside-out origin for the eukaryotic cell

Baum, David A.; Baum, Buzz

doi:10.1186/s12915-014-0076-2

Cited by 150 publications

(158 citation statements)

References 208 publications

(270 reference statements)

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“…Baum and Baum have recently turned this sequence of events 'inside-out', suggesting that ''.eukaryotes evolved from a prokaryotic cell with a single bounding membrane that extended extracellular protrusions that fused to give rise to the cytoplasm and endomembrane system'' [133]. It was these protrusions that surrounded the bacterial ancestors of mitochondria.…”

Section: The Essence Of An Organellementioning

confidence: 98%

Endosymbiosis and Eukaryotic Cell Evolution

2015

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Understanding the evolution of eukaryotic cellular complexity is one of the grand challenges of modern biology. It has now been firmly established that mitochondria and plastids, the classical membrane-bound organelles of eukaryotic cells, evolved from bacteria by endosymbiosis. In the case of mitochondria, evidence points very clearly to an endosymbiont of α-proteobacterial ancestry. The precise nature of the host cell that partnered with this endosymbiont is, however, very much an open question. And while the host for the cyanobacterial progenitor of the plastid was undoubtedly a fully-fledged eukaryote, how - and how often - plastids moved from one eukaryote to another during algal diversification is vigorously debated. In this article I frame modern views on endosymbiotic theory in a historical context, highlighting the transformative role DNA sequencing played in solving early problems in eukaryotic cell evolution, and posing key unanswered questions emerging from the age of comparative genomics.

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Section: The Essence Of An Organellementioning

confidence: 98%

Endosymbiosis and Eukaryotic Cell Evolution

2015

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“…5-10) or as part of a broader view of eukaryotic cell evolution (e.g., refs. [11][12][13][14], interest in this subject is unlikely to wane any time soon.…”

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confidence: 99%

Mosaic nature of the mitochondrial proteome: Implications for the origin and evolution of mitochondria

Gray

2015

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

155

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Comparative studies of the mitochondrial proteome have identified a conserved core of proteins descended from the α-proteobacterial endosymbiont that gave rise to the mitochondrion and was the source of the mitochondrial genome in contemporary eukaryotes. A surprising result of phylogenetic analyses is the relatively small proportion (10-20%) of the mitochondrial proteome displaying a clear α-proteobacterial ancestry. A large fraction of mitochondrial proteins typically has detectable homologs only in other eukaryotes and is presumed to represent proteins that emerged specifically within eukaryotes. A further significant fraction of the mitochondrial proteome consists of proteins with homologs in prokaryotes, but without a robust phylogenetic signal affiliating them with specific prokaryotic lineages. The presumptive evolutionary source of these proteins is quite different in contending models of mitochondrial origin.nderstanding the origin and evolution of the mitochondrion remains a challenge, despite the flood of relevant biochemical, cell and molecular biological, and phylogenetic data and insights that have accumulated in the almost five decades since the modern resurrection (1, 2) of the long-standing endosymbiont hypothesis: the idea that this organelle is a tamed and highly reworked endosymbiotic bacterium. The abundance of information bearing on eukaryotic cell evolution (particularly and most recently sequence data) and differences over how the data are analyzed and interpreted have prompted a plethora of often-conflicting ideas about when and how, within an endosymbiotic context, the mitochondrion originated (3, 4). Considering the spate of recent papers dealing with various aspects of mitochondrial origin and evolution either explicitly (e.g., refs. 5-

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“…eukaryote evolution | mitochondria | vesicles | dynamin | FtsZ E ukaryotes arose through the acquisition of mitochondria by an archaeal host cell about 2 billion y ago (1,2), a watershed moment in the evolution of the modern compartmentalized cell plan (3). A second transformative endosymbiotic event, the acquisition of a cyanobacterium by a eukaryotic host to form chloroplasts, gave rise to the photosynthetic eukaryotic lineages (4).…”

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Ancient dynamin segments capture early stages of host–mitochondrial integration

Purkanti

Thattai

2015

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

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Eukaryotic cells use dynamins-mechano-chemical GTPases-to drive the division of endosymbiotic organelles. Here we probe early steps of mitochondrial and chloroplast endosymbiosis by tracing the evolution of dynamins. We develop a parsimony-based phylogenetic method for protein sequence reconstruction, with deep time resolution. Using this, we demonstrate that dynamins diversify through the punctuated transformation of sequence segments on the scale of secondary-structural elements. We find examples of segments that have remained essentially unchanged from the 1.8-billion-y-old last eukaryotic common ancestor to the present day. Stitching these together, we reconstruct three ancestral dynamins: The first is nearly identical to the ubiquitous mitochondrial division dynamins of extant eukaryotes, the second is partially preserved in the myxovirus-resistance-like dynamins of metazoans, and the third gives rise to the cytokinetic dynamins of amoebozoans and plants and to chloroplast division dynamins. The reconstructed sequences, combined with evolutionary models and published functional data, suggest that the ancestral mitochondrial division dynamin also mediated vesicle scission. This bifunctional protein duplicated into specialized mitochondrial and vesicle variants at least three independent times-in alveolates, green algae, and the ancestor of fungi and metazoans-accompanied by the loss of the ancient prokaryotic mitochondrial division protein FtsZ. Remarkably, many extant species that retain FtsZ also retain the predicted ancestral bifunctional dynamin. The mitochondrial division apparatus of such organisms, including amoebozoans, red algae, and stramenopiles, seems preserved in a nearprimordial form.eukaryote evolution | mitochondria | vesicles | dynamin | FtsZ E ukaryotes arose through the acquisition of mitochondria by an archaeal host cell about 2 billion y ago (1, 2), a watershed moment in the evolution of the modern compartmentalized cell plan (3). A second transformative endosymbiotic event, the acquisition of a cyanobacterium by a eukaryotic host to form chloroplasts, gave rise to the photosynthetic eukaryotic lineages (4). As the endosymbionts became integrated with their hosts, their growth and division became regulated by host-cellular machinery (5). Proteins of the dynamin superfamily were central to this process: Mitochondria and chloroplasts originally divided using a constricting ring of the prokaryotic cytoskeletal protein FtsZ, but dynamins have been recruited to these roles in all extant eukaryotes (6, 7). By reconstructing the evolutionary history of dynamins, we can probe the process of endosymbiont integration.The dynamin superfamily is diverse (8, 9), and different dynamin variants remodel membranes at different cellular locations (Table S1 and primary references therein). A major class of dynamins is essential for mitochondrial and peroxisomal division. Another large group drives the scission of clathrin-coated vesicles in organisms such as fungi and alveolates. A related group, the socal...

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An inside-out origin for the eukaryotic cell

Cited by 150 publications

References 208 publications

Endosymbiosis and Eukaryotic Cell Evolution

Endosymbiosis and Eukaryotic Cell Evolution

Mosaic nature of the mitochondrial proteome: Implications for the origin and evolution of mitochondria

Ancient dynamin segments capture early stages of host–mitochondrial integration

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