The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin

Molecular Biology and Evolution
Xavier Grau-BovéIñaki Ruiz-Trillo

Abstract

The origin of the eukaryotic cell is one of the most important transitions in the history of life. However, the emergence and early evolution of eukaryotes remains poorly understood. Recent data have shown that the last eukaryotic common ancestor (LECA) was much more complex than previously thought. The LECA already had the genetic machinery encoding the endomembrane apparatus, spliceosome, nuclear pore, and myosin and kinesin cytoskeletal motors. It is unclear, however, when the functional regulation of these cellular components evolved. Here, we address this question by analyzing the origin and evolution of the ubiquitin (Ub) signaling system, one of the most important regulatory layers in eukaryotes. We delineated the evolution of the whole Ub, Small-Ub-related MOdifier (SUMO), and Ub-fold modifier 1 (Ufm1) signaling networks by analyzing representatives from all major eukaryotic, bacterial, and archaeal lineages. We found that the Ub toolkit had a pre-eukaryotic origin and is present in three extant archaeal groups. The pre-eukaryotic Ub toolkit greatly expanded during eukaryogenesis, through massive gene innovation and diversification of protein domain architectures. This resulted in a LECA with essentially all of the Ub-r...Continue Reading

References

Jan 1, 1991·Bio Systems·T Cavalier-Smith
Jun 1, 1990·Proceedings of the National Academy of Sciences of the United States of America·C R WoeseM L Wheelis
Mar 1, 1987·Nature·T Cavalier-Smith
Jul 9, 1998·Journal of Molecular Biology·P BayerJ Becker
Jan 27, 1999·Bioinformatics·Sean R Eddy
Feb 29, 2000·The Journal of Biological Chemistry·H Saitoh, J Hinchey
Aug 10, 2000·Nature Cell Biology·Mark Hochstrasser
Sep 7, 2001·Annual Review of Microbiology·Eugene V KooninL Aravind
Aug 10, 2002·Proceedings of the National Academy of Sciences of the United States of America·Jennifer M GagneRichard D Vierstra
Apr 9, 2004·The EMBO Journal·Masaaki KomatsuKeiji Tanaka
Jun 11, 2004·Annual Review of Biochemistry·Erica S Johnson
Sep 2, 2004·Nature Reviews. Molecular Cell Biology·Timothy Cardozo, Michele Pagano
Sep 21, 2004·Annual Review of Plant Biology·Jan Smalle, Richard D Vierstra
Dec 2, 2004·Biochimica Et Biophysica Acta·Andrew R WillemsMike Tyers
Dec 2, 2004·Biochimica Et Biophysica Acta·Alexander Y Amerik, Mark Hochstrasser
Jan 13, 2005·Plant Physiology·Sophia L StoneJudy Callis
Jan 22, 2005·Molecular Biology and Evolution·Lesley Collins, David Penny
Feb 3, 2005·Nature Reviews. Molecular Cell Biology·Matthew D Petroski, Raymond J Deshaies
Jun 3, 2005·Nature·David Reverter, Christopher D Lima
Sep 24, 2005·The FEBS Journal·Hedvig TordaiLászló Patthy
Apr 18, 2006·Proceedings. Biological Sciences·Elizabeth A SnellPeter W H Holland
May 9, 2006·Current Opinion in Structural Biology·L AravindEugene V Koonin
Jun 7, 2006·Annual Review of Cell and Developmental Biology·Oliver KerscherMark Hochstrasser
Aug 22, 2006·Plant Physiology·Thomas ColbyHans-Peter Stuible
Jan 2, 2007·Biochimica Et Biophysica Acta·Alan J Whitmarsh
Jan 16, 2007·Science·Debdyuti Mukhopadhyay, Howard Riezman
May 15, 2007·Oncogene·A G TurjanskiJ S Gutkind
May 15, 2007·Trends in Biochemical Sciences·Debaditya Mukhopadhyay, Mary Dasso
Oct 11, 2007·Current Biology : CB·Maja AdamskaBernard M Degnan
Nov 17, 2007·Bioinformatics·Yassen AssenovMario Albrecht
Jan 31, 2008·Genome Research·Malay Kumar BasuEugene V Koonin
Mar 28, 2008·Molecular Biology and Evolution·Si Quang Le, Olivier Gascuel
Aug 22, 2008·Trends in Ecology & Evolution·Svetlana A Shabalina, Eugene V Koonin
Jan 20, 2009·Briefings in Bioinformatics·Malay Kumar BasuIgor B Rogozin
Mar 28, 2009·Nature·Mark Hochstrasser
May 14, 2009·Nature Reviews. Molecular Cell Biology·Daniela Rotin, Sharad Kumar
May 20, 2009·Journal of Molecular Evolution·Caroline MichelleChristian R Andres
Jun 6, 2009·Annual Review of Biochemistry·Raymond J Deshaies, Claudio A P Joazeiro
Jun 16, 2009·Cellular Microbiology·Thomas SpallekVera Göhre
Jun 16, 2009·Journal of Molecular Evolution·Ignacio Marín
Jun 19, 2009·Bioinformatics·Nicolas LartillotSamuel Blanquart
Oct 15, 2009·BMC Evolutionary Biology·Eve GazaveEmmanuelle Renard
Nov 21, 2009·BMC Evolutionary Biology·Ignacio Marín
Dec 17, 2009·BMC Bioinformatics·Christiam CamachoThomas L Madden
Dec 23, 2009·Progress in Biophysics and Molecular Biology·Krupa DeshmukhNarayanaswamy Srinivasan
Jan 8, 2010·Nature·Matthew A HumbardJulie A Maupin-Furlow
Feb 24, 2010·BMC Evolutionary Biology·Ignacio Marín
Jun 29, 2010·Cellular and Molecular Life Sciences : CMLS·Andrew BrighouseMark C Field
Sep 8, 2010·Nature Reviews. Microbiology·Kira S MakarovaEugene V Koonin
Oct 29, 2010·BMC Evolutionary Biology·Ignacio Marín
Nov 26, 2010·Nature Reviews. Molecular Cell Biology·Jaclyn R Gareau, Christopher D Lima
Dec 15, 2010·Bioinformatics·Michael E SmootTrey Ideker
Feb 10, 2011·Nature Communications·Kanako TatsumiMasaaki Komatsu
Feb 22, 2011·Bioinformatics·Diego DarribaDavid Posada
Mar 5, 2011·Annual Review of Plant Biology·Zhihua Hua, Richard D Vierstra
Aug 24, 2011·The Journal of Cell Biology·Bill Wickstead, Keith Gull
Dec 1, 2011·Nucleic Acids Research·Marco PuntaRobert D Finn
Dec 3, 2011·Molecular Biology and Evolution·Romain Derelle, B Franz Lang
Mar 13, 2012·Annual Review of Biochemistry·Annemarthe G van der Veen, Hidde L Ploegh
Oct 2, 2012·The Journal of Eukaryotic Microbiology·Sina M AdlFrederick W Spiegel
Oct 26, 2012·Proceedings. Biological Sciences·Tom A WilliamsT Martin Embley
Nov 24, 2012·Nature Reviews. Molecular Cell Biology·Christopher M HickeyMark Hochstrasser
Jan 19, 2013·Molecular Biology and Evolution·Kazutaka Katoh, Daron M Standley
Apr 10, 2013·Trends in Cell Biology·Hirofumi HarashimaArp Schnittger
Jun 27, 2013·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Yuri I Wolf, Eugene V Koonin
Jul 23, 2013·PloS One·Ignacio Marín
Jul 31, 2013·Critical Reviews in Biochemistry and Molecular Biology·V Lila KoumandouMark C Field
Nov 21, 2013·Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution·Raphael B Di Roberto, Sergio G Peisajovich
Nov 28, 2013·Proceedings of the National Academy of Sciences of the United States of America·Alex de MendozaIñaki Ruiz-Trillo
Dec 18, 2013·Nature·Tom A WilliamsT Martin Embley
Jan 21, 2014·Genome Biology and Evolution·Arnau Sebé-PedrósIñaki Ruiz-Trillo
Feb 11, 2014·Current Biology : CB·Ding HeSandra L Baldauf

Citations

Apr 18, 2015·Proceedings of the National Academy of Sciences of the United States of America·Austin Booth, W Ford Doolittle
Sep 2, 2015·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Eugene V Koonin
May 24, 2016·Trends in Ecology & Evolution·Maureen A O'MalleyIñaki Ruiz-Trillo
Feb 9, 2017·Genome Biology and Evolution·Caitlyn VlasschaertDouglas A Gray
Nov 11, 2017·Nature Reviews. Microbiology·Laura EmeThijs J G Ettema
May 9, 2018·The Plant Journal : for Cell and Molecular Biology·Zhihua HuaWilliam Vu
Jul 21, 2017·ELife·Xavier Grau-BovéIñaki Ruiz-Trillo
May 28, 2019·Proceedings of the National Academy of Sciences of the United States of America·Eelco C TromerBerend Snel
Feb 24, 2018·Annals of Botany·František Baluška, Sherrie Lyons
Apr 1, 2017·Scientific Reports·Prasanth PadalaReuven Wiener
Mar 15, 2018·BMC Biology·Raphaël MéheustEric Bapteste
May 20, 2021·Frontiers in Molecular Biosciences·Yangchun Frank Chen, Yu Xia

Methods Mentioned

BETA
ubiquitination
PCA
RNA-Seq

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