Elusive data underlying debate at the prokaryote-eukaryote divide

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.

Keywords: Bioenergetics; Eukaryogenesis; Major evolutionary transitions; Mitochondria; Ribosomes.

Fig. 1

Ribosomes per cell and cell volume. a Boxplots of the distribution of prokaryotic and eukaryotic ‘ribosomes per cell and cell volume’-ratios. The Wilcoxon ranksum test rejected the null hypothesis that the eukaryotic and prokaryotic samples are part of the same continuous distribution with ρ=0.0003. b Ribosomes per cell versus cell volume. Blue crosses: Prokaryotes. Orange circles: Eukaryotes. Excluding Ostreococcus tauri, there is a gap of approximately 1.5 orders of magnitude between prokaryotic and eukaryotic cell volumes, indicating the fundamental differences in prokaryotic and eukaryotic nature. All values were taken from Lynch and Marinov [1] Appendix 1-Table 3. c Replot of Fig. 1b, only showing data points where both cell volume and the number of ribosomes per cell could be verified by the provided references in Lynch and Marinov [1]