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      The origins of cellular life

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          Abstract

          All life on earth can be naturally classified into cellular life forms and virus-like selfish elements, the latter being fully dependent on the former for their reproduction. Cells are reproducers that not only replicate their genome but also reproduce the cellular organization that depends on semipermeable, energy-transforming membranes and cannot be recovered from the genome alone, under the famous dictum of Rudolf Virchow, Omnis cellula e cellula. In contrast, simple selfish elements are replicators that can complete their life cycles within the host cell starting from genomic RNA or DNA alone. The origin of the cellular organization is the central and perhaps the hardest problem of evolutionary biology. I argue that the origin of cells can be understood only in conjunction with the origin and evolution of selfish genetic elements. A scenario of precellular evolution is presented that involves cohesion of the genomes of the emerging cellular life forms from primordial pools of small genetic elements that eventually segregated into hosts and parasites. I further present a model of the coevolution of primordial membranes and membrane proteins, discuss protocellular and non-cellular models of early evolution, and examine the habitats on the primordial earth that could have been conducive to precellular evolution and the origin of cells.

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          Most cited references127

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          Extreme genome reduction in symbiotic bacteria.

          Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.
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            Hydrothermal vents and the origin of life.

            Submarine hydrothermal vents are geochemically reactive habitats that harbour rich microbial communities. There are striking parallels between the chemistry of the H(2)-CO(2) redox couple that is present in hydrothermal systems and the core energy metabolic reactions of some modern prokaryotic autotrophs. The biochemistry of these autotrophs might, in turn, harbour clues about the kinds of reactions that initiated the chemistry of life. Hydrothermal vents thus unite microbiology and geology to breathe new life into research into one of biology's most important questions - what is the origin of life?
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              Genome streamlining in a cosmopolitan oceanic bacterium.

              The SAR11 clade consists of very small, heterotrophic marine alpha-proteobacteria that are found throughout the oceans, where they account for about 25% of all microbial cells. Pelagibacter ubique, the first cultured member of this clade, has the smallest genome and encodes the smallest number of predicted open reading frames known for a free-living microorganism. In contrast to parasitic bacteria and archaea with small genomes, P. ubique has complete biosynthetic pathways for all 20 amino acids and all but a few cofactors. P. ubique has no pseudogenes, introns, transposons, extrachromosomal elements, or inteins; few paralogs; and the shortest intergenic spacers yet observed for any cell.
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                Author and article information

                Contributors
                koonin@ncbi.nlm.nih.gov
                Journal
                Antonie Van Leeuwenhoek
                Antonie Van Leeuwenhoek
                Antonie Van Leeuwenhoek
                Springer International Publishing (Cham )
                0003-6072
                1572-9699
                23 April 2014
                2014
                : 106
                : 1
                : 27-41
                Affiliations
                GRID grid.280285.5, ISNI 0000000405077840, National Center for Biotechnology Information, , National Library of Medicine, National Institute of Health, ; Bethesda, MD 20894 USA
                Article
                169
                10.1007/s10482-014-0169-5
                7087693
                24756907
                bbf3f846-b2d2-4bd0-ba57-58252750e5a9
                © Springer International Publishing Switzerland (outside the USA) 2014

                This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

                History
                : 14 March 2014
                : 3 April 2014
                Categories
                Invited Review
                Custom metadata
                © Springer International Publishing Switzerland 2014

                Microbiology & Virology
                rna world,viruses,selfish elements,membrane evolution,cellular organization

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