Thermococcus coalescens sp. nov., a cell-fusing hyperthermophilic archaeon from Suiyo Seamount

Kuwabara, Tomohiko; Minaba, Masaomi; Iwayama, Yukihiro; Inouye, Isao; Nakashima, Miwako; Marumo, Katsumi; Maruyama, Akihiko; Sugai, Akihiko; Itoh, Toshihiro; Ishibashi, Jun Ichiro; Urabe, Tetsuro; Kamekura, Masahiro

doi:10.1099/ijs.0.63432-0

Cited by 44 publications

(38 citation statements)

References 44 publications

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“…If these cells divide, a very curious property of the archaeal host cell could rescue progeny: Archaeal cells can fuse. That archaeal cells fuse has been reported for the crenarchaeote Sulfolobus (Schleper et al 1995), for several Thermococcus species (Kuwabara et al 2005), and the euryarchaeote Haloferax (Naor and Gophna 2014). It is thus a property found within both the crenarchaeal and the euryarchaeal groups, hence attributable to our host without need for invention.…”

Section: Ordering Events At the Prokaryote–eukaryote Transitionmentioning

confidence: 78%

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Garg

Martin

2016

Genome Biol Evol

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Theories for the origin of sex traditionally start with an asexual mitosing cell and add recombination, thereby deriving meiosis from mitosis. Though sex was clearly present in the eukaryote common ancestor, the order of events linking the origin of sex and the origin of mitosis is unknown. Here, we present an evolutionary inference for the origin of sex starting with a bacterial ancestor of mitochondria in the cytosol of its archaeal host. We posit that symbiotic association led to the origin of mitochondria and gene transfer to host’s genome, generating a nucleus and a dedicated translational compartment, the eukaryotic cytosol, in which—by virtue of mitochondria—metabolic energy was not limiting. Spontaneous protein aggregation (monomer polymerization) and Adenosine Tri-phosphate (ATP)-dependent macromolecular movement in the cytosol thereby became selectable, giving rise to continuous microtubule-dependent chromosome separation (reduction division). We propose that eukaryotic chromosome division arose in a filamentous, syncytial, multinucleated ancestor, in which nuclei with insufficient chromosome numbers could complement each other through mRNA in the cytosol and generate new chromosome combinations through karyogamy. A syncytial (or coenocytic, a synonym) eukaryote ancestor, or Coeca, would account for the observation that the process of eukaryotic chromosome separation is more conserved than the process of eukaryotic cell division. The first progeny of such a syncytial ancestor were likely equivalent to meiospores, released into the environment by the host’s vesicle secretion machinery. The natural ability of archaea (the host) to fuse and recombine brought forth reciprocal recombination among fusing (syngamy and karyogamy) progeny—sex—in an ancestrally meiotic cell cycle, from which the simpler haploid and diploid mitotic cell cycles arose. The origin of eukaryotes was the origin of vertical lineage inheritance, and sex was required to keep vertically evolving lineages viable by rescuing the incipient eukaryotic lineage from Muller’s ratchet. The origin of mitochondria was, in this view, the decisive incident that precipitated symbiosis-specific cell biological problems, the solutions to which were the salient features that distinguish eukaryotes from prokaryotes: A nuclear membrane, energetically affordable ATP-dependent protein–protein interactions in the cytosol, and a cell cycle involving reduction division and reciprocal recombination (sex).

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Section: Ordering Events At the Prokaryote–eukaryote Transitionmentioning

confidence: 78%

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Garg

Martin

2016

Genome Biol Evol

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“…The basic machinery required might have been a property of the host. It is a curiously underpublicized observation that various archaea can fuse their cells (55,107) and that, in some haloarchaea, fusion is accompanied by recombination (108) whereas, in others, only recombination is observed (109). One needs to be careful not to (over-)state that "archaea have sex," but, in some rare documented examples, they do undergo outright cell fusion (an otherwise curious property of gametes) and, in some rarer cases, recombination and fusion are observed (108).…”

Section: Supernumerary Symbionts or Inherited Chimerism?mentioning

confidence: 99%

Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes

Nelson-Sathi

Roettger

et al. 2015

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

119

105

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Endosymbiotic theory in eukaryotic-cell evolution rests upon a foundation of three cornerstone partners-the plastid (a cyanobacterium), the mitochondrion (a proteobacterium), and its host (an archaeon)-and carries a corollary that, over time, the majority of genes once present in the organelle genomes were relinquished to the chromosomes of the host (endosymbiotic gene transfer). However, notwithstanding eukaryote-specific gene inventions, single-gene phylogenies have never traced eukaryotic genes to three single prokaryotic sources, an issue that hinges crucially upon factors influencing phylogenetic inference. In the age of genomes, single-gene trees, once used to test the predictions of endosymbiotic theory, now spawn new theories that stand to eventually replace endosymbiotic theory with descriptive, gene tree-based variants featuring supernumerary symbionts: prokaryotic partners distinct from the cornerstone trio and whose existence is inferred solely from single-gene trees. We reason that the endosymbiotic ancestors of mitochondria and chloroplasts brought into the eukaryotic-and plant and algal-lineage a genome-sized sample of genes from the proteobacterial and cyanobacterial pangenomes of their respective day and that, even if molecular phylogeny were artifact-free, sampling prokaryotic pangenomes through endosymbiotic gene transfer would lead to inherited chimerism. Recombination in prokaryotes (transduction, conjugation, transformation) differs from recombination in eukaryotes (sex). Prokaryotic recombination leads to pangenomes, and eukaryotic recombination leads to vertical inheritance. Viewed from the perspective of endosymbiotic theory, the critical transition at the eukaryote origin that allowed escape from Muller's ratchet-the origin of eukaryotic recombination, or sex-might have required surprisingly little evolutionary innovation.endosymbiosis | evolution | mitochondria | lateral gene transfer | plastids

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“…Woese 1987Woese , 1998. (Kuwabara et al 2005). Note that wholesale combination of genomes by fusions and fissions is not only far more intense than the horizontal transfer of individual genes from donor cell to acceptor cell.…”

Section: Cellularization (A) Surface Lipophilizationmentioning

confidence: 99%

From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya

Wächtershäuser¹

2006

Phil. Trans. R. Soc. B

248

225

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The theory of a chemoautotrophic origin of life in a volcanic iron-sulphur world postulates a pioneer organism at sites of reducing volcanic exhalations. The pioneer organism is characterized by a composite structure with an inorganic substructure and an organic superstructure. Within the surfaces of the inorganic substructure iron, cobalt, nickel and other transition metal centres with sulphido, carbonyl and other ligands were catalytically active and promoted the growth of the organic superstructure through carbon fixation, driven by the reducing potential of the volcanic exhalations. This pioneer metabolism was reproductive by an autocatalytic feedback mechanism. Some organic products served as ligands for activating catalytic metal centres whence they arose. The unitary structure-function relationship of the pioneer organism later gave rise to two major strands of evolution: cellularization and emergence of the genetic machinery. This early phase of evolution ended with segregation of the domains Bacteria, Archaea and Eukarya from a rapidly evolving population of pre-cells. Thus, life started with an initial, direct, deterministic chemical mechanism of evolution giving rise to a later, indirect, stochastic, genetic mechanism of evolution and the upward evolution of life by increase of complexity is grounded ultimately in the synthetic redox chemistry of the pioneer organism.

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Thermococcus coalescens sp. nov., a cell-fusing hyperthermophilic archaeon from Suiyo Seamount

Cited by 44 publications

References 44 publications

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes

From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya

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