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      Elusive data underlying debate at the prokaryote-eukaryote divide

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          Abstract

          Background

          The origin of eukaryotic cells was an important transition in evolution. The factors underlying the origin and evolutionary success of the eukaryote lineage are still discussed. One camp argues that mitochondria were essential for eukaryote origin because of the unique configuration of internalized bioenergetic membranes that they conferred to the common ancestor of all known eukaryotic lineages. A recent paper by Lynch and Marinov concluded that mitochondria were energetically irrelevant to eukaryote origin, a conclusion based on analyses of previously published numbers of various molecules and ribosomes per cell and cell volumes as a presumed proxy for the role of mitochondria in evolution. Their numbers were purportedly extracted from the literature.

          Results

          We have examined the numbers upon which the recent study was based. We report that for a sample of 80 numbers that were purportedly extracted from the literature and that underlie key inferences of the recent study, more than 50% of the values do not exist in the cited papers to which the numbers are attributed. The published result cannot be independently reproduced. Other numbers that the recent study reports differ inexplicably from those in the literature to which they are ascribed. We list the discrepancies between the recently published numbers and the purported literature sources of those numbers in a head to head manner so that the discrepancies are readily evident, although the source of error underlying the discrepancies remains obscure.

          Conclusion

          The data purportedly supporting the view that mitochondria had no impact upon eukaryotic evolution data exhibits notable irregularities. The paper in question evokes the impression that the published numbers are of up to seven significant digit accuracy, when in fact more than half the numbers are nowhere to be found in the literature to which they are attributed. Though the reasons for the discrepancies are unknown, it is important to air these issues, lest the prominent paper in question become a point source of a snowballing error through the literature or become interpreted as a form of evidence that mitochondria were irrelevant to eukaryote evolution.

          Reviewers

          This article was reviewed by Eric Bapteste, Jianzhi Zhang and Martin Lercher.

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          Most cited references50

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          Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation.

          We report a method for large-scale absolute protein expression measurements (APEX) and apply it to estimate the relative contributions of transcriptional- and translational-level gene regulation in the yeast and Escherichia coli proteomes. APEX relies upon correcting each protein's mass spectrometry sampling depth (observed peptide count) by learned probabilities for identifying the peptides. APEX abundances agree with measurements from controls, western blotting, flow cytometry and two-dimensional gels, as well as known correlations with mRNA abundances and codon bias, providing absolute protein concentrations across approximately three to four orders of magnitude. Using APEX, we demonstrate that 73% of the variance in yeast protein abundance (47% in E. coli) is explained by mRNA abundance, with the number of proteins per mRNA log-normally distributed about approximately 5,600 ( approximately 540 in E. coli) protein molecules/mRNA. Therefore, levels of both eukaryotic and prokaryotic proteins are set per mRNA molecule and independently of overall protein concentration, with >70% of yeast gene expression regulation occurring through mRNA-directed mechanisms.
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            A “Proteomic Ruler” for Protein Copy Number and Concentration Estimation without Spike-in Standards*

            Absolute protein quantification using mass spectrometry (MS)-based proteomics delivers protein concentrations or copy numbers per cell. Existing methodologies typically require a combination of isotope-labeled spike-in references, cell counting, and protein concentration measurements. Here we present a novel method that delivers similar quantitative results directly from deep eukaryotic proteome datasets without any additional experimental steps. We show that the MS signal of histones can be used as a “proteomic ruler” because it is proportional to the amount of DNA in the sample, which in turn depends on the number of cells. As a result, our proteomic ruler approach adds an absolute scale to the MS readout and allows estimation of the copy numbers of individual proteins per cell. We compare our protein quantifications with values derived via the use of stable isotope labeling by amino acids in cell culture and protein epitope signature tags in a method that combines spike-in protein fragment standards with precise isotope label quantification. The proteomic ruler approach yields quantitative readouts that are in remarkably good agreement with results from the precision method. We attribute this surprising result to the fact that the proteomic ruler approach omits error-prone steps such as cell counting or protein concentration measurements. The proteomic ruler approach is readily applicable to any deep eukaryotic proteome dataset—even in retrospective analysis—and we demonstrate its usefulness with a series of mouse organ proteomes.
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              The hydrogen hypothesis for the first eukaryote.

              A new hypothesis for the origin of eukaryotic cells is proposed, based on the comparative biochemistry of energy metabolism. Eukaryotes are suggested to have arisen through symbiotic association of an anaerobic, strictly hydrogen-dependent, strictly autotrophic archaebacterium (the host) with a eubacterium (the symbiont) that was able to respire, but generated molecular hydrogen as a waste product of anaerobic heterotrophic metabolism. The host's dependence upon molecular hydrogen produced by the symbiont is put forward as the selective principle that forged the common ancestor of eukaryotic cells.
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                Author and article information

                Contributors
                marie.gerlitz@hhu.de
                michael.knopp@hhu.de
                nils.kapust@hhu.de
                xavier@hhu.de
                bill@hhu.de
                Journal
                Biol Direct
                Biol. Direct
                Biology Direct
                BioMed Central (London )
                1745-6150
                3 October 2018
                3 October 2018
                2018
                : 13
                : 21
                Affiliations
                ISNI 0000 0001 2176 9917, GRID grid.411327.2, Institute for Molecular Evolution, , Heinrich-Heine-University Düsseldorf, ; Universitätsstr. 1, 40225 Düsseldorf, Germany
                Article
                221
                10.1186/s13062-018-0221-x
                6888934
                31196150
                60aadd28-2554-41a0-88cc-89a9f597d8d3
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 22 March 2018
                : 16 August 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: 666053
                Funded by: FundRef http://dx.doi.org/10.13039/501100001736, German-Israeli Foundation for Scientific Research and Development;
                Award ID: I-1321-203.13/2015
                Funded by: FundRef http://dx.doi.org/10.13039/501100001663, Volkswagen Foundation;
                Award ID: 93 046
                Categories
                Comment
                Custom metadata
                © The Author(s) 2018

                Life sciences
                eukaryogenesis,mitochondria,ribosomes,bioenergetics,major evolutionary transitions
                Life sciences
                eukaryogenesis, mitochondria, ribosomes, bioenergetics, major evolutionary transitions

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