Mind the gaps in cellular evolution

McInerney, James O.; O’Connell, Mary J.

doi:10.1038/nature21113

Cited by 7 publications

(4 citation statements)

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“…Due to a lack of enriched cultures, it is still not yet clear whether these metagenomic proteins and gene families all belong to one organism or several. Some of the reported protein family distributions are patchy among the Asgard superphylum, which complicates speculations regarding their overall function (265). More importantly, these few proteins and domains fall short of the long list of components that are required to underpin endomembrane flux and phagocytosis (118,119) (Table 1).…”

Section: New Archaeal Genomes and Inferring Phenotype From Single Genesmentioning

confidence: 99%

The Physiology of Phagocytosis in the Context of Mitochondrial Origin

Martin

Tielens

Mentel

et al. 2017

Microbiol Mol Biol Rev

102

132

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How mitochondria came to reside within the cytosol of their host has been debated for 50 years. Though current data indicate that the last eukaryote common ancestor possessed mitochondria and was a complex cell, whether mitochondria or complexity came first in eukaryotic evolution is still discussed. In autogenous models (complexity first), the origin of phagocytosis poses the limiting step at eukaryote origin, with mitochondria coming late as an undigested growth substrate. In symbiosis-based models (mitochondria first), the host was an archaeon, and the origin of mitochondria was the limiting step at eukaryote origin, with mitochondria providing bacterial genes, ATP synthesis on internalized bioenergetic membranes, and mitochondrion-derived vesicles as the seed of the eukaryote endomembrane system. Metagenomic studies are uncovering new host-related archaeal lineages that are reported as complex or phagocytosing, although images of such cells are lacking. Here we review the physiology and components of phagocytosis in eukaryotes, critically inspecting the concept of a phagotrophic host. From ATP supply and demand, a mitochondrion-lacking phagotrophic archaeal fermenter would have to ingest about 34 times its body weight in prokaryotic prey to obtain enough ATP to support one cell division. It would lack chemiosmotic ATP synthesis at the plasma membrane, because phagocytosis and chemiosmosis in the same membrane are incompatible. It would have lived from amino acid fermentations, because prokaryotes are mainly protein. Its ATP yield would have been impaired relative to typical archaeal amino acid fermentations, which involve chemiosmosis. In contrast, phagocytosis would have had great physiological benefit for a mitochondrion-bearing cell.

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Section: New Archaeal Genomes and Inferring Phenotype From Single Genesmentioning

confidence: 99%

The Physiology of Phagocytosis in the Context of Mitochondrial Origin

Martin

Tielens

Mentel

et al. 2017

Microbiol Mol Biol Rev

102

132

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“…are descended from an alpha-proteobacterium that was involved in a merger with another cell [31][32][33][34]. Recent analysis of metagenomic data suggests that the other partner in this merger was an early member of the ASGARD group of archaebacteria [35,36]. The nascent eukaryotic cell seems to have been able to combine several features of both partners in this merger, in order to produce new versions of DNA replication, transcription, RNA processing, translation and metabolism [31].…”

Section: Merging Of Evolving Objectsmentioning

confidence: 99%

The role of public goods in planetary evolution

McInerney

Erwin

2017

Phil. Trans. R. Soc. A.

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Biological public goods are broadly shared within an ecosystem and readily available. They appear to be widespread and may have played important roles in the history of life on Earth. Of particular importance to events in the early history of life are the roles of public goods in the merging of genomes, protein domains and even cells. We suggest that public goods facilitated the origin of the eukaryotic cell, a classic major evolutionary transition. The recognition of genomic public goods challenges advocates of a direct graph view of phylogeny, and those who deny that any useful phylogenetic signal persists in modern genomes. Ecological spillovers generate public goods that provide new ecological opportunities.This article is part of the themed issue 'Reconceptualizing the origins of life'.

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“…Doubts of a different nature are coming to bear upon the issue, however. That is, some researchers now doubt that the metagenomic data currently being interpreted as indicating complex archaea really reflect the existence of complex archaea [14,30,[33][34][35][36][37][38]. We know that eukaryotes are complex because we can observe their complexity both under the microscope and in everyday life.…”

mentioning

confidence: 99%

“…For the sake of reasoning, let us assume for a moment that doubts about the existence of complex archaea [14,30,[33][34][35][36][37][38] are justified. We would then ask the following question.…”

mentioning

confidence: 99%

Archaeal Histone Contributions to the Origin of Eukaryotes

Brunk

Martin

2019

Trends in Microbiology

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The eukaryotic lineage arose from bacterial and archaeal cells that underwent a symbiotic merger. At the origin of the eukaryote lineage, the bacterial partner contributed genes, metabolic energy, and the building blocks of the endomembrane system. What did the archaeal partner donate that made the eukaryotic experiment a success? The archaeal partner provided the potential for complex information processing. Archaeal histones were crucial in that regard by providing the basic functional unit with which eukaryotes organize DNA into nucleosomes, exert epigenetic control of gene expression, transcribe genes with CCAAT-box promoters, and a manifest cell cycle with condensed chromosomes. While mitochondrial energy lifted energetic constraints on eukaryotic protein production, histone-based chromatin organization paved the path to eukaryotic genome complexity, a critical hurdle en route to the evolution of complex cells. Eukaryotes from Prokaryotes: Symbiotic Contributions HighlightsThe last common ancestor of eukaryotes had mitochondria, pointing to hostsymbiont interactions at eukaryote origin. Mitochondria contributed energy, genes, and membranes to the eukaryotic lineage. What did the archaeal host contribute?Recent metagenomic studies propose that close relatives of the archaeal host exist that are 'complex' (phagocytosing) and that the archaeal host brought that complexity to eukaryotes.Yet complex archaea have not been found, and there are doubts that the metagenomic archaeal data represent truly complex archaea.Alternatively, histones could have been the key archaeal contribution to eukaryote complexity.In eukaryotes, histone modifications link gene expression to the physiological state of the cell via carbon-, energy-, and nitrogen-sensing through regulators such as AMPK, GCN2, and TOR. The Archaeal ContributionSince their discovery, archaea have been implicated as relatives of the host lineage at the origin of eukaryogenesis and mitochondria [18,19]. There is now much discussion about the possibility that complex, phagocytosing archaea might be yet discovered in nature, based on metagenomic data [20][21][22]. In that view, the contribution of archaea is unequivocal: the archaeal host brought preformed complexity to the eukaryotic lineage. Indeed, the possibility that some archaea or archaeal relatives might possess a primitive cytoskeleton has been discussed for decades [23][24][25][26].

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Mind the gaps in cellular evolution

Cited by 7 publications

References 9 publications

The Physiology of Phagocytosis in the Context of Mitochondrial Origin

The Physiology of Phagocytosis in the Context of Mitochondrial Origin

The role of public goods in planetary evolution

Archaeal Histone Contributions to the Origin of Eukaryotes

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