Literature DB >> 25883267

Eukaryogenesis, how special really?

Austin Booth1, W Ford Doolittle2.   

Abstract

Eukaryogenesis is widely viewed as an improbable evolutionary transition uniquely affecting the evolution of life on this planet. However, scientific and popular rhetoric extolling this event as a singularity lacks rigorous evidential and statistical support. Here, we question several of the usual claims about the specialness of eukaryogenesis, focusing on both eukaryogenesis as a process and its outcome, the eukaryotic cell. We argue in favor of four ideas. First, the criteria by which we judge eukaryogenesis to have required a genuinely unlikely series of events 2 billion years in the making are being eroded by discoveries that fill in the gaps of the prokaryote:eukaryote "discontinuity." Second, eukaryogenesis confronts evolutionary theory in ways not different from other evolutionary transitions in individuality; parallel systems can be found at several hierarchical levels. Third, identifying which of several complex cellular features confer on eukaryotes a putative richer evolutionary potential remains an area of speculation: various keys to success have been proposed and rejected over the five-decade history of research in this area. Fourth, and perhaps most importantly, it is difficult and may be impossible to eliminate eukaryocentric bias from the measures by which eukaryotes as a whole are judged to have achieved greater success than prokaryotes as a whole. Overall, we question whether premises of existing theories about the uniqueness of eukaryogenesis and the greater evolutionary potential of eukaryotes have been objectively formulated and whether, despite widespread acceptance that eukaryogenesis was "special," any such notion has more than rhetorical value.

Keywords:  endosymbiosis; eukaryogenesis; evolutionary theory; major transitions

Mesh:

Year:  2015        PMID: 25883267      PMCID: PMC4547297          DOI: 10.1073/pnas.1421376112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  51 in total

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Journal:  Symbiosis       Date:  1991       Impact factor: 2.268

3.  Cell biology. Irremediable complexity?

Authors:  Michael W Gray; Julius Lukes; John M Archibald; Patrick J Keeling; W Ford Doolittle
Journal:  Science       Date:  2010-11-12       Impact factor: 47.728

4.  Reproduction, symbiosis, and the eukaryotic cell.

Authors:  Peter Godfrey-Smith
Journal:  Proc Natl Acad Sci U S A       Date:  2015-04-14       Impact factor: 11.205

5.  The frailty of adaptive hypotheses for the origins of organismal complexity.

Authors:  Michael Lynch
Journal:  Proc Natl Acad Sci U S A       Date:  2007-05-09       Impact factor: 11.205

Review 6.  The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes.

Authors:  Eugene V Koonin; Natalya Yutin
Journal:  Cold Spring Harb Perspect Biol       Date:  2014-04-01       Impact factor: 10.005

7.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme.

Authors:  S J Gould; R C Lewontin
Journal:  Proc R Soc Lond B Biol Sci       Date:  1979-09-21

8.  Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis.

Authors:  Filip Husnik; Naruo Nikoh; Ryuichi Koga; Laura Ross; Rebecca P Duncan; Manabu Fujie; Makiko Tanaka; Nori Satoh; Doris Bachtrog; Alex C C Wilson; Carol D von Dohlen; Takema Fukatsu; John P McCutcheon
Journal:  Cell       Date:  2013-06-20       Impact factor: 41.582

9.  Origins of major archaeal clades correspond to gene acquisitions from bacteria.

Authors:  Shijulal Nelson-Sathi; Filipa L Sousa; Mayo Roettger; Nabor Lozada-Chávez; Thorsten Thiergart; Arnold Janssen; David Bryant; Giddy Landan; Peter Schönheit; Bettina Siebers; James O McInerney; William F Martin
Journal:  Nature       Date:  2014-10-15       Impact factor: 49.962

Review 10.  Endosymbiotic theory for organelle origins.

Authors:  Verena Zimorski; Chuan Ku; William F Martin; Sven B Gould
Journal:  Curr Opin Microbiol       Date:  2014-10-10       Impact factor: 7.934

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  26 in total

1.  The bioenergetic costs of a gene.

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Journal:  Proc Natl Acad Sci U S A       Date:  2015-11-02       Impact factor: 11.205

2.  Eukaryotes really are special, and mitochondria are why.

Authors:  Nick Lane; William F Martin
Journal:  Proc Natl Acad Sci U S A       Date:  2015-08-17       Impact factor: 11.205

3.  Reply to Lane and Martin: Being and becoming eukaryotes.

Authors:  Austin Booth; W Ford Doolittle
Journal:  Proc Natl Acad Sci U S A       Date:  2015-08-17       Impact factor: 11.205

4.  Symbiosis becoming permanent: Survival of the luckiest.

Authors:  Patrick J Keeling; John P McCutcheon; W Ford Doolittle
Journal:  Proc Natl Acad Sci U S A       Date:  2015-08-18       Impact factor: 11.205

Review 5.  Early Microbial Evolution: The Age of Anaerobes.

Authors:  William F Martin; Filipa L Sousa
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-12-18       Impact factor: 10.005

Review 6.  Eukaryotes first: how could that be?

Authors:  Carlos Mariscal; W Ford Doolittle
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-26       Impact factor: 6.237

7.  The Origin(s) of Cell(s): Pre-Darwinian Evolution from FUCAs to LUCA : To Carl Woese (1928-2012), for his Conceptual Breakthrough of Cellular Evolution.

Authors:  Shiping Tang
Journal:  J Mol Evol       Date:  2021-06-25       Impact factor: 2.395

Review 8.  Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria).

Authors:  Thomas Cavalier-Smith; Ema E-Yung Chao
Journal:  Protoplasma       Date:  2020-01-03       Impact factor: 3.356

9.  Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis.

Authors:  Filip Husnik; John P McCutcheon
Journal:  Proc Natl Acad Sci U S A       Date:  2016-08-29       Impact factor: 11.205

10.  The Asgard Archaeal-Unique Contribution to Protein Families of the Eukaryotic Common Ancestor Was 0.3.

Authors:  Michael Knopp; Simon Stockhorst; Mark van der Giezen; Sriram G Garg; Sven B Gould
Journal:  Genome Biol Evol       Date:  2021-06-08       Impact factor: 3.416

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