Archaeal Histone Contributions to the Origin of Eukaryotes
2019; Elsevier BV; Volume: 27; Issue: 8 Linguagem: Inglês
10.1016/j.tim.2019.04.002
ISSN1878-4380
AutoresClifford F. Brunk, William Martin,
Tópico(s)RNA and protein synthesis mechanisms
ResumoThe last common ancestor of eukaryotes had mitochondria, pointing to host–symbiont 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 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. 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. The origin of eukaryotes remains one of evolution's more pressing unresolved questions; however, it is beginning to yield some of its secrets. Over the past several decades, perspectives on eukaryogenesis have undergone a significant transformation [1.McInerney J.O. et al.The hybrid nature of the Eukaryota and a consilient view of life on Earth.Nat. Rev. Microbiol. 2014; 12: 449-455Crossref PubMed Scopus (70) Google Scholar]. Mitochondria are now thought to have been present in the eukaryote common ancestor [2.Betts H.C. et al.Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin.Nat. Ecol. Evol. 2018; 2: 1556-1562Crossref PubMed Scopus (6) Google Scholar, 3.Judson O.P. The energy expansions of evolution.Nat. Ecol. Evol. 2017; 1: 0138Crossref PubMed Google Scholar], and the broad outlines of eukaryote lineage origin have increasingly come to include the concept of symbiosis [4.Zillig W. et al.Did eukaryotes originate by a fusion event?.Endocyt. Cell Res. 1989; 6: 1-25Google Scholar, 5.Martin W. Müller M. 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Initially, nucleosomes were viewed as static structural elements facilitating the manipulation of the DNA; the role of histones in organizing eukaryotic DNA into nucleosomes provides a basis for enhanced control of gene expression. Having a greatly expanded DNA content dramatically increases the necessity for control of genetic expression in eukaryotes well beyond the prokaryotic mechanisms for regulation of gene expression. Within the nucleos
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