{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,21]],"date-time":"2026-04-21T05:55:04Z","timestamp":1776750904540,"version":"3.51.2"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1008623","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T00:00:00Z","timestamp":1616457600000}}],"reference-count":112,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2021,3,8]],"date-time":"2021-03-08T00:00:00Z","timestamp":1615161600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"XSEDE","award":["TG-BCS190003"],"award-info":[{"award-number":["TG-BCS190003"]}]},{"DOI":"10.13039\/100000104","name":"National Aeronautics and Space Administration","doi-asserted-by":"publisher","award":["80NSSC19M0069"],"award-info":[{"award-number":["80NSSC19M0069"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["MRI1427949"],"award-info":[{"award-number":["MRI1427949"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["NSF Solicitation 16-570"],"award-info":[{"award-number":["NSF Solicitation 16-570"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>In this study, we used a computational approach to investigate the early evolutionary history of a system of proteins that, together, embed and translocate other proteins across cell membranes. Cell membranes comprise the basis for cellularity, which is an ancient, fundamental organizing principle shared by all organisms and a key innovation in the evolution of life on Earth. Two related requirements for cellularity are that organisms are able to both embed proteins into membranes and translocate proteins across membranes. One system that accomplishes these tasks is the signal recognition particle (SRP) system, in which the core protein components are the paralogs, FtsY and Ffh. Complementary to the SRP system is the Sec translocation channel, in which the primary channel-forming protein is SecY. We performed phylogenetic analyses that strongly supported prior inferences that FtsY, Ffh, and SecY were all present by the time of the last universal common ancestor of life, the LUCA, and that the ancestor of FtsY and Ffh existed before the LUCA. Further, we combined ancestral sequence reconstruction and protein structure and function prediction to show that the LUCA had an SRP system and Sec translocation channel that were similar to those of extant organisms. We also show that the ancestor of Ffh and FtsY that predated the LUCA was more similar to FtsY than Ffh but could still have comprised a rudimentary protein translocation system on its own. Duplication of the ancestor of FtsY and Ffh facilitated the specialization of FtsY as a membrane bound receptor and Ffh as a cytoplasmic protein that could bind nascent proteins with specific membrane-targeting signal sequences. Finally, we analyzed amino acid frequencies in our ancestral sequence reconstructions to infer that the ancestral Ffh\/FtsY protein likely arose prior to or just after the completion of the canonical genetic code. Taken together, our results offer a window into the very early evolutionary history of cellularity.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1008623","type":"journal-article","created":{"date-parts":[[2021,3,8]],"date-time":"2021-03-08T18:39:00Z","timestamp":1615228740000},"page":"e1008623","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":24,"title":["The very early evolution of protein translocation across membranes"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3215-1201","authenticated-orcid":true,"given":"AJ","family":"Harris","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1115-3697","authenticated-orcid":true,"given":"Aaron David","family":"Goldman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2021,3,8]]},"reference":[{"key":"pcbi.1008623.ref001","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1038\/374227a0","article-title":"The major evolutionary transitions","volume":"374","author":"E Szathm\u00e1ry","year":"1995","journal-title":"Nature"},{"key":"pcbi.1008623.ref002","doi-asserted-by":"crossref","first-page":"6854","DOI":"10.1073\/pnas.95.12.6854","article-title":"The universal ancestor.","volume":"95","author":"C Woese","year":"1998","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"pcbi.1008623.ref003","doi-asserted-by":"crossref","DOI":"10.1007\/s11084-017-9542-5","article-title":"Environmental adaptation from the origin of life to the last universal common ancestor","volume":"48","author":"MD Cantine","year":"2018","journal-title":"Origins of Life and Evolution of Biospheres"},{"key":"pcbi.1008623.ref004","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1007\/s00239-020-09961-1","article-title":"The coevolution of cellularity and metabolism following the origin of life","volume":"88","author":"YA Takagi","year":"2020","journal-title":"Journal of Molecular Evolution"},{"key":"pcbi.1008623.ref005","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1038\/320634a0","article-title":"The signal sequence of nascent preprolactin interacts with the 54K polypeptide of the signal recognition particle","volume":"320","author":"T Kurzchalia","year":"1986","journal-title":"Nature"},{"key":"pcbi.1008623.ref006","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1126\/science.1701272","article-title":"An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle","volume":"250","author":"M Poritz","year":"1990","journal-title":"Science"},{"key":"pcbi.1008623.ref007","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1093\/nar\/28.6.1365","article-title":"Assembly of archaeal signal recognition particle from recombinant components","volume":"28","author":"SH Bhuiyan","year":"2000","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref008","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1038\/340482a0","article-title":"Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle","volume":"340","author":"HD Bernstein","year":"1989","journal-title":"Nature"},{"key":"pcbi.1008623.ref009","doi-asserted-by":"crossref","first-page":"15650","DOI":"10.1074\/jbc.270.26.15650","article-title":"An amino-terminal domain containing hydrophobic and hydrophilic sequences binds the signal recognition particle receptor \u03b1 subunit to the \u03b2 subunit on the endoplasmic reticulum membrane","volume":"270","author":"JC Young","year":"1995","journal-title":"Journal of Biological Chemistry"},{"key":"pcbi.1008623.ref010","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0167-4781(96)00236-9","article-title":"Identification of a gene in the euryarchaeal Thermococcus species AN1 encoding a protein homologous to the alpha subunit of the eukaryal signal recognition particle (SRP) receptor.","volume":"1351","author":"RS Ronimus","year":"1997","journal-title":"Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression."},{"key":"pcbi.1008623.ref011","doi-asserted-by":"crossref","first-page":"1640","DOI":"10.1126\/science.288.5471.1640","article-title":"Role of 4.5S RNA in assembly of the bacterial signal recognition particle with its receptor","volume":"288","author":"P Peluso","year":"2000","journal-title":"Science"},{"key":"pcbi.1008623.ref012","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1074\/jbc.M116.752931","article-title":"Co-evolution of Two GTPases enables efficient protein targeting in an RNA-less chloroplast signal recognition particle pathway","volume":"292","author":"S Chandrasekar","year":"2017","journal-title":"Journal of Biological Chemistry"},{"key":"pcbi.1008623.ref013","doi-asserted-by":"crossref","first-page":"3479","DOI":"10.1093\/emboj\/cdg337","article-title":"Structure, function and evolution of the signal recognition particle","volume":"22","author":"K Nagai","year":"2003","journal-title":"The EMBO journal"},{"key":"pcbi.1008623.ref014","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1006\/jmbi.2001.5378","article-title":"Classification and evolution of P-loop GTPases and related ATPases11Edited by J. Thornton","volume":"317","author":"DD Leipe","year":"2002","journal-title":"Journal of Molecular Biology"},{"key":"pcbi.1008623.ref015","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1038\/nrm2689","article-title":"It takes two to tango: regulation of G proteins by dimerization","volume":"10","author":"R Gasper","year":"2009","journal-title":"Nature Reviews Molecular Cell Biology"},{"key":"pcbi.1008623.ref016","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1016\/j.molcel.2013.10.005","article-title":"The Structural Basis of FtsY Recruitment and GTPase Activation by SRP RNA","volume":"52","author":"F Voigts-Hoffmann","year":"2013","journal-title":"Molecular Cell"},{"key":"pcbi.1008623.ref017","doi-asserted-by":"crossref","first-page":"1232","DOI":"10.1126\/science.287.5456.1232","article-title":"Crystal Structure of the Ribonucleoprotein Core of the Signal Recognition Particle","volume":"287","author":"RT Batey","year":"2000","journal-title":"Science"},{"key":"pcbi.1008623.ref018","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1038\/nsmb.1994","article-title":"Structural basis of signal-sequence recognition by the signal recognition particle.","volume":"18","author":"T Hainzl","year":"2011","journal-title":"Nature Structural & Molecular Biology."},{"key":"pcbi.1008623.ref019","doi-asserted-by":"crossref","first-page":"32176","DOI":"10.1074\/jbc.M705430200","article-title":"Escherichia coli signal recognition particle receptor FtsY contains an essential and autonomous membrane-binding amphipathic helix","volume":"282","author":"R Parlitz","year":"2007","journal-title":"Journal of Biological Chemistry"},{"key":"pcbi.1008623.ref020","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1016\/j.jmb.2008.01.040","article-title":"A cleavable N-terminal membrane anchor is involved in membrane binding of the Escherichia coli SRP receptor","volume":"377","author":"B Weiche","year":"2008","journal-title":"Journal of Molecular Biology"},{"key":"pcbi.1008623.ref021","doi-asserted-by":"crossref","first-page":"2728","DOI":"10.1091\/mbc.e07-02-0117","article-title":"The signal recognition particle (SRP) RNA links conformational changes in the SRP to protein targeting.","volume":"18","author":"N Bradshaw","year":"2007","journal-title":"Molecular biology of the cell"},{"key":"pcbi.1008623.ref022","doi-asserted-by":"crossref","first-page":"23489","DOI":"10.1074\/jbc.M110.212340","article-title":"Lipids trigger a conformational switch that regulates signal recognition particle (SRP)-mediated protein targeting.","volume":"286","author":"G Stjepanovic","year":"2011","journal-title":"Journal of Biological Chemistry"},{"key":"pcbi.1008623.ref023","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1080\/09687680701416570","article-title":"Structure and function of the bacterial Sec translocon (Review).","volume":"24","author":"VAM Gold","year":"2007","journal-title":"Molecular Membrane Biology"},{"key":"pcbi.1008623.ref024","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1128\/JB.188.4.1251-1259.2006","article-title":"Archaeal and bacterial SecD and SecF homologs exhibit striking structural and functional conservation","volume":"188","author":"NJ Hand","year":"2006","journal-title":"Journal of Bacteriology"},{"key":"pcbi.1008623.ref025","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.bbamcr.2004.02.009","article-title":"Driessen AJM The protein-conducting channel SecYEG","volume":"1694","author":"AKJ Veenendaal","year":"2004","journal-title":"Biochimica et Biophysica Acta (BBA)\u2014Molecular Cell Research."},{"key":"pcbi.1008623.ref026","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1038\/340478a0","article-title":"Homology of 54K protein of signal-recognition particle, docking protein and two E. coli proteins with putative GTP\u2013binding domains","volume":"340","author":"K R\u00f6misch","year":"1989","journal-title":"Nature"},{"key":"pcbi.1008623.ref027","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.sbi.2005.03.007","article-title":"Targeting proteins to membranes: structure of the signal recognition particle","volume":"15","author":"PF Egea","year":"2005","journal-title":"Current Opinion in Structural Biology"},{"key":"pcbi.1008623.ref028","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1007\/PL00006407","article-title":"The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery","volume":"47","author":"S Gribaldo","year":"1998","journal-title":"Journal of Molecular Evolution"},{"key":"pcbi.1008623.ref029","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/S0005-2736(02)00662-4","article-title":"The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions","volume":"1609","author":"TB Cao","year":"2003","journal-title":"Biochimica et Biophysica Acta (BBA)\u2013Biomembranes."},{"key":"pcbi.1008623.ref030","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/nature12352","article-title":"Insights into the phylogeny and coding potential of microbial dark matter","volume":"499","author":"C Rinke","year":"2013","journal-title":"Nature"},{"key":"pcbi.1008623.ref031","doi-asserted-by":"crossref","DOI":"10.1002\/9781118960608.pbm00026","volume-title":"Thermodesulfobacteria phy. nov.","author":"GM Garrity","year":"2015"},{"key":"pcbi.1008623.ref032","doi-asserted-by":"crossref","first-page":"16048","DOI":"10.1038\/nmicrobiol.2016.48","article-title":"A new view of the tree of life","volume":"1","author":"LA Hug","year":"2016","journal-title":"Nature Microbiology"},{"key":"pcbi.1008623.ref033","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1038\/nature21031","article-title":"Asgard archaea illuminate the origin of eukaryotic cellular complexity","volume":"541","author":"K Zaremba-Niedzwiedzka","year":"2017","journal-title":"Nature"},{"key":"pcbi.1008623.ref034","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"SF Altschul","year":"1990","journal-title":"Journal of Molecular Biology"},{"key":"pcbi.1008623.ref035","doi-asserted-by":"crossref","first-page":"9355","DOI":"10.1073\/pnas.86.23.9355","article-title":"Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes","volume":"86","author":"N Iwabe","year":"1989","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"pcbi.1008623.ref036","doi-asserted-by":"crossref","first-page":"D309","DOI":"10.1093\/nar\/gky1085","article-title":"eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses","volume":"47","author":"J Huerta-Cepas","year":"2019","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref037","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1002\/(SICI)1097-0134(199707)28:3<405::AID-PROT10>3.0.CO;2-L","article-title":"Pfam: a comprehensive database of protein domain families based on seed alignments.","volume":"28","author":"EL Sonnhammer","year":"1997","journal-title":"Proteins: Structure, Function, and Bioinformatics."},{"key":"pcbi.1008623.ref038","doi-asserted-by":"crossref","first-page":"D427","DOI":"10.1093\/nar\/gky995","article-title":"The Pfam protein families database in 2019","volume":"47","author":"S El-Gebali","year":"2018","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref039","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1093\/bioinformatics\/14.4.378","article-title":"SOSUI: classification and secondary structure prediction system for membrane proteins","volume":"14","author":"T Hirokawa","year":"1998","journal-title":"Bioinformatics (Oxford, England)."},{"key":"pcbi.1008623.ref040","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/nprot.2010.5","article-title":"I-TASSER: a unified platform for automated protein structure and function prediction.","volume":"5","author":"A Roy","year":"2010","journal-title":"Nature Protocols."},{"key":"pcbi.1008623.ref041","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/j.jmb.2007.09.061","article-title":"Structure of the chloroplast signal recognition particle (SRP) receptor: domain arrangement modulates SRP\u2013receptor interaction.","volume":"375","author":"S Chandrasekar","year":"2008","journal-title":"Journal of Molecular Biology"},{"key":"pcbi.1008623.ref042","doi-asserted-by":"crossref","first-page":"4819","DOI":"10.1105\/tpc.112.102996","article-title":"Evolution from the Prokaryotic to the Higher Plant Chloroplast Signal Recognition Particle: The Signal Recognition Particle RNA Is Conserved in Plastids of a Wide Range of Photosynthetic Organisms","volume":"24","author":"C Tr\u00e4ger","year":"2012","journal-title":"The Plant Cell"},{"key":"pcbi.1008623.ref043","first-page":"150","volume-title":"Characterization of the ftsYEX operon of Escherichia coli","author":"B Graham","year":"2002"},{"key":"pcbi.1008623.ref044","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1093\/oxfordjournals.molbev.a026114","article-title":"Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes","volume":"16","author":"T Itoh","year":"1999","journal-title":"Molecular Biology and Evolution"},{"key":"pcbi.1008623.ref045","doi-asserted-by":"crossref","first-page":"2872","DOI":"10.1038\/s41467-019-10918-2","article-title":"Structure of the substrate-engaged SecA-SecY protein translocation machine","volume":"10","author":"C Ma","year":"2019","journal-title":"Nature communications"},{"key":"pcbi.1008623.ref046","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.1073\/pnas.54.6.1546","article-title":"On the evolution of the genetic code","volume":"54","author":"CR Woese","year":"1965","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"pcbi.1008623.ref047","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/0022-2836(68)90392-6","article-title":"The origin of the genetic code","volume":"38","author":"FHC Crick","year":"1968","journal-title":"Journal of Molecular Biology"},{"key":"pcbi.1008623.ref048","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0968-0004(99)01392-4","article-title":"Selection, history and chemistry: the three faces of the genetic code","volume":"24","author":"RD Knight","year":"1999","journal-title":"Trends in Biochemical Sciences"},{"key":"pcbi.1008623.ref049","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/S0168-9525(99)01730-8","article-title":"The origin of the genetic code: amino acids as cofactors in an RNA world","volume":"15","author":"E Szathm\u00e1ry","year":"1999","journal-title":"Trends in Genetics"},{"key":"pcbi.1008623.ref050","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1093\/oxfordjournals.molbev.a026331","article-title":"Early fixation of an optimal genetic code","volume":"17","author":"SJ Freeland","year":"2000","journal-title":"Molecular Biology and Evolution"},{"key":"pcbi.1008623.ref051","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/1745-6150-5-15","article-title":"The evolution and functional repertoire of translation proteins following the origin of life","volume":"5","author":"AD Goldman","year":"2010","journal-title":"Biology Direct"},{"key":"pcbi.1008623.ref052","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S0378-1119(00)00476-5","article-title":"Consensus temporal order of amino acids and evolution of the triplet code","volume":"261","author":"EN Trifonov","year":"2000","journal-title":"Gene"},{"key":"pcbi.1008623.ref053","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1038\/nature03306","article-title":"A universal trend of amino acid gain and loss in protein evolution","volume":"433","author":"IK Jordan","year":"2005","journal-title":"Nature"},{"key":"pcbi.1008623.ref054","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/s00239-015-9672-1","article-title":"Ancestral reconstruction of a pre-LUCA aminoacyl-tRNA synthetase ancestor supports the late addition of trp to the genetic code","volume":"80","author":"GP Fournier","year":"2015","journal-title":"Journal of Molecular Evolution"},{"key":"pcbi.1008623.ref055","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1038\/nature08015","article-title":"Microbial habitability of the Hadean Earth during the late heavy bombardment","volume":"459","author":"O Abramov","year":"2009","journal-title":"Nature"},{"key":"pcbi.1008623.ref056","first-page":"1","article-title":"Earliest signs of life on land preserved in ca. 3.5 Ga hot spring deposits","volume":"8","author":"T Djokic","year":"2017","journal-title":"Nature Communications"},{"key":"pcbi.1008623.ref057","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1038\/nature21377","article-title":"Evidence for early life in Earth\u2019s oldest hydrothermal vent precipitates","volume":"543","author":"MS Dodd","year":"2017","journal-title":"Nature"},{"key":"pcbi.1008623.ref058","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1038\/nature24019","article-title":"Early trace of life from 3.95 Ga sedimentary rocks in Labrador, Canada.","volume":"549","author":"T Tashiro","year":"2017","journal-title":"Nature"},{"key":"pcbi.1008623.ref059","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1089\/ast.2017.1674","article-title":"Constraining the time interval for the origin of life on Earth.","volume":"18","author":"BK Pearce","year":"2018","journal-title":"Astrobiology"},{"key":"pcbi.1008623.ref060","doi-asserted-by":"crossref","first-page":"1556","DOI":"10.1038\/s41559-018-0644-x","article-title":"Integrated genomic and fossil evidence illuminates life\u2019s early evolution and eukaryote origin","volume":"2","author":"HC Betts","year":"2018","journal-title":"Nature ecology & evolution"},{"key":"pcbi.1008623.ref061","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/BF01808285","article-title":"Amphiphilic components of the Murchison carbonaceous chondrite: surface properties and membrane formation","volume":"19","author":"DW Deamer","year":"1989","journal-title":"Origins of Life and Evolution of the Biosphere"},{"key":"pcbi.1008623.ref062","doi-asserted-by":"crossref","first-page":"6210","DOI":"10.1021\/la047028z","article-title":"From decanoate micelles to decanoic acid\/dodecylbenzenesulfonate vesicles.","volume":"21","author":"T Namani","year":"2005","journal-title":"Langmuir"},{"key":"pcbi.1008623.ref063","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/0168-9525(96)20010-1","article-title":"Non-orthologous gene displacement. Trends in genetics","volume":"12","author":"EV Koonin","year":"1996","journal-title":"TIG"},{"key":"pcbi.1008623.ref064","doi-asserted-by":"crossref","first-page":"1295","DOI":"10.1093\/gbe\/evx088","article-title":"Unique phylogenetic distributions of the Ska and Dam1 complexes support functional analogy and suggest multiple parallel displacements of Ska by Dam1","volume":"9","author":"JJE van Hooff","year":"2017","journal-title":"Genome Biology and Evolution"},{"key":"pcbi.1008623.ref065","doi-asserted-by":"crossref","first-page":"977","DOI":"10.3390\/biom10070977","article-title":"Survey and validation of tRNA modifications and their corresponding genes in Bacillus subtilis sp subtilis strain 168.","volume":"10","author":"V de Cr\u00e9cy-Lagard","year":"2020","journal-title":"Biomolecules"},{"key":"pcbi.1008623.ref066","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1046\/j.1365-2958.1999.01497.x","article-title":"Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins","volume":"33","author":"P Forterre","year":"1999","journal-title":"Molecular Microbiology"},{"key":"pcbi.1008623.ref067","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1016\/j.tig.2012.03.010","article-title":"Oxytricha as a modern analog of ancient genome evolution","volume":"28","author":"AD Goldman","year":"2012","journal-title":"Trends in Genetics"},{"key":"pcbi.1008623.ref068","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1101\/gr.6454307","article-title":"Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world","volume":"17","author":"M Wang","year":"2007","journal-title":"Genome Research"},{"key":"pcbi.1008623.ref069","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms10471","article-title":"Structures of the E. coli translating ribosome with SRP and its receptor and with the translocon","volume":"7","author":"A Jomaa","year":"2016","journal-title":"Nature Communications"},{"key":"pcbi.1008623.ref070","doi-asserted-by":"crossref","first-page":"15470","DOI":"10.1038\/ncomms15470","article-title":"Structure of the quaternary complex between SRP, SR, and translocon bound to the translating ribosome.","volume":"8","author":"A Jomaa","year":"2017","journal-title":"Nature Communications."},{"key":"pcbi.1008623.ref071","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1534\/genetics.104.037051","article-title":"Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution","volume":"169","author":"X He","year":"2005","journal-title":"Genetics"},{"key":"pcbi.1008623.ref072","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1186\/1471-2148-5-28","article-title":"Subfunctionalization of duplicated genes as a transition state to neofunctionalization","volume":"5","author":"S Rastogi","year":"2005","journal-title":"BMC Evolutionary Biology"},{"key":"pcbi.1008623.ref073","doi-asserted-by":"crossref","first-page":"e1002752","DOI":"10.1371\/journal.pcbi.1002752","article-title":"Comparative analysis of RNA families reveals distinct repertoires for each domain of life","volume":"8","author":"MP Hoeppner","year":"2012","journal-title":"PLoS Computational Biology"},{"key":"pcbi.1008623.ref074","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1007\/PL00006280","article-title":"Relics from the RNA world","volume":"46","author":"DC Jeffares","year":"1998","journal-title":"Journal of Molecular Evolution"},{"key":"pcbi.1008623.ref075","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/0092-8674(81)90136-7","article-title":"The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis","volume":"23","author":"D Engelman","year":"1981","journal-title":"Cell"},{"key":"pcbi.1008623.ref076","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1111\/j.1574-6976.1995.tb00201.x","article-title":"Major coat proteins of bacteriophage Pf3 and M13 as model systems for Sec-independent protein transport","volume":"17","author":"A Kuhn","year":"1995","journal-title":"FEMS Microbiology Reviews"},{"key":"pcbi.1008623.ref077","doi-asserted-by":"crossref","first-page":"16914","DOI":"10.1038\/srep16914","article-title":"Spontaneous membrane-translocating peptides: Influence of peptide self-aggregation and cargo polarity","volume":"5","author":"S Macchi","year":"2015","journal-title":"Scientific Reports"},{"key":"pcbi.1008623.ref078","doi-asserted-by":"crossref","first-page":"D158","DOI":"10.1093\/nar\/gkw1099","article-title":"UniProt: the universal protein knowledgebase.","volume":"45","author":"The UniProt Consortium","year":"2017","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref079","doi-asserted-by":"crossref","first-page":"e9605","DOI":"10.1371\/journal.pone.0009605","article-title":"The complete genome sequence of Haloferax volcanii DS2, a model archaeon.","volume":"5","author":"AL Hartman","year":"2010","journal-title":"PLOS One."},{"key":"pcbi.1008623.ref080","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.tim.2018.10.004","article-title":"Haloferax volcanii.","volume":"27","author":"M Pohlschroder","year":"2019","journal-title":"Trends in Microbiology"},{"key":"pcbi.1008623.ref081","doi-asserted-by":"crossref","first-page":"D733","DOI":"10.1093\/nar\/gkv1189","article-title":"Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation.","volume":"44","author":"NA O\u2019Leary","year":"2015","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref082","doi-asserted-by":"crossref","first-page":"D5","DOI":"10.1093\/nar\/gkn741","article-title":"Database resources of the National Center for Biotechnology Information","volume":"37","author":"EW Sayers","year":"2009","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref083","doi-asserted-by":"crossref","first-page":"D26","DOI":"10.1093\/nar\/gkn723","article-title":"GenBank.","volume":"37","author":"DA Benson","year":"2009","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref084","first-page":"1376","article-title":"Structural basis for the molecular evolution of SRP-GTPase activation by protein. Nature Structural &","volume":"18","author":"G Bange","year":"2011","journal-title":"Molecular Biology"},{"key":"pcbi.1008623.ref085","doi-asserted-by":"crossref","first-page":"1647","DOI":"10.1093\/bioinformatics\/bts199","article-title":"Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data","volume":"28","author":"M Kearse","year":"2012","journal-title":"Bioinformatics"},{"key":"pcbi.1008623.ref086","doi-asserted-by":"crossref","first-page":"3059","DOI":"10.1093\/nar\/gkf436","article-title":"MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform","volume":"30","author":"K Katoh","year":"2002","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref087","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1093\/nar\/gki198","article-title":"MAFFT version 5: improvement in accuracy of multiple sequence alignment","volume":"33","author":"K Katoh","year":"2005","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref088","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT multiple sequence alignment software version 7: improvements in performance and usability","volume":"30","author":"K Katoh","year":"2013","journal-title":"Molecular Biology and Evolution"},{"key":"pcbi.1008623.ref089","doi-asserted-by":"crossref","first-page":"2553","DOI":"10.1093\/molbev\/msu236","article-title":"ExaBayes: massively parallel Bayesian tree inference for the whole-genome era","volume":"31","author":"AJ Aberer","year":"2014","journal-title":"Molecular Biology and Evolution"},{"key":"pcbi.1008623.ref090","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1093\/oxfordjournals.molbev.a003851","article-title":"A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach","volume":"18","author":"N Goldman","year":"2001","journal-title":"Molecular Biology and Evolution"},{"key":"pcbi.1008623.ref091","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1093\/bioinformatics\/17.8.754","article-title":"MRBAYES: Bayesian inference of phylogenetic trees","volume":"17","author":"JP Huelsenbeck","year":"2001","journal-title":"Bioinformatics"},{"key":"pcbi.1008623.ref092","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1093\/bioinformatics\/btg180","article-title":"MrBayes 3: Bayesian phylogenetic inference under mixed models","volume":"19","author":"F Ronquist","year":"2003","journal-title":"Bioinformatics"},{"key":"pcbi.1008623.ref093","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1093\/sysbio\/sys029","article-title":"MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space","volume":"61","author":"F Ronquist","year":"2012","journal-title":"Systematic Biology"},{"key":"pcbi.1008623.ref094","doi-asserted-by":"crossref","unstructured":"Rambaut A, Drummond A. Tracer. 1.4 ed. 2007","DOI":"10.1371\/journal.pbio.0040088"},{"key":"pcbi.1008623.ref095","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1186\/1471-2148-7-214","article-title":"BEAST: Bayesian evolutionary analysis by sampling trees","volume":"7","author":"A Drummond","year":"2007","journal-title":"BMC Evolutionary Biology"},{"key":"pcbi.1008623.ref096","doi-asserted-by":"crossref","first-page":"e1003537","DOI":"10.1371\/journal.pcbi.1003537","article-title":"BEAST 2: a software platform for Bayesian evolutionary analysis","volume":"10","author":"R Bouckaert","year":"2014","journal-title":"PLoS Computational Biology"},{"key":"pcbi.1008623.ref097","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1093\/oxfordjournals.molbev.a026334","article-title":"Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis","volume":"17","author":"J Castresana","year":"2000","journal-title":"Molecular Biology and Evolution"},{"key":"pcbi.1008623.ref098","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1080\/10635150701472164","article-title":"Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments","volume":"56","author":"G Talavera","year":"2007","journal-title":"Systematic Biology"},{"key":"pcbi.1008623.ref099","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1111\/j.2041-210X.2011.00169.x","article-title":"phytools: an R package for phylogenetic comparative biology (and other things).","volume":"3","author":"LJ Revell","year":"2012","journal-title":"Methods in Ecology and Evolution"},{"key":"pcbi.1008623.ref100","article-title":"On merging Acer sections Rubra and Hyptiocarpa: Molecular and morphological evidence.","volume":"9","author":"AJ Harris","year":"2017","journal-title":"PhytoKeys"},{"key":"pcbi.1008623.ref101","doi-asserted-by":"crossref","first-page":"W580","DOI":"10.1093\/nar\/gks498","article-title":"FastML: a web server for probabilistic reconstruction of ancestral sequences","volume":"40","author":"H Ashkenazy","year":"2012","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref102","doi-asserted-by":"crossref","DOI":"10.1038\/msb.2011.75","article-title":"Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.","volume":"7","author":"F Sievers","year":"2011","journal-title":"Molecular systems biology"},{"key":"pcbi.1008623.ref103","first-page":"207","volume-title":"SeqinR 1.0\u20132: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis.","author":"D Charif","year":"2007"},{"key":"pcbi.1008623.ref104","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1093\/nar\/28.1.235","article-title":"The Protein Data Bank","volume":"28","author":"HM Berman","year":"2000","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref105","first-page":"39","article-title":"The RCSB Protein Data Bank: redesigned web site and web services","author":"P Rose","year":"2010","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1008623.ref106","doi-asserted-by":"crossref","first-page":"4673","DOI":"10.1093\/nar\/22.22.4673","article-title":"CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice","volume":"22","author":"JD Thompson","year":"1994","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1008623.ref107","first-page":"571","volume-title":"Protein identification and analysis tools on the ExPASy server.","author":"E Gasteiger","year":"2005"},{"key":"pcbi.1008623.ref108","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1038\/75556","article-title":"Gene Ontology: tool for the unification of biology.","volume":"25","author":"Gene Ontology Consortium","year":"2000","journal-title":"Nature Genetics."},{"key":"pcbi.1008623.ref109","doi-asserted-by":"crossref","first-page":"D258","DOI":"10.1093\/nar\/gkh036","article-title":"The Gene Ontology (GO) database and informatics resource.","volume":"32","author":"Gene Ontology Consortium","year":"2004","journal-title":"Nucleic acids research"},{"key":"pcbi.1008623.ref110","doi-asserted-by":"crossref","first-page":"D1096","DOI":"10.1093\/nar\/gks966","article-title":"BioLiP: a semi-manually curated database for biologically relevant ligand\u2013protein interactions","volume":"41","author":"J Yang","year":"2012","journal-title":"Nucleic Acids Research"},{"key":"pcbi.1008623.ref111","first-page":"82","article-title":"Pymol: An open-source molecular graphics tool.","volume":"40","author":"WL DeLano","year":"2002","journal-title":"CCP4 Newsletter on Protein Crystallography"},{"key":"pcbi.1008623.ref112","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1093\/bioinformatics\/btq706","article-title":"phangorn: phylogenetic analysis in R.","volume":"27","author":"KP Schliep","year":"2010","journal-title":"Bioinformatics"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1008623","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T00:00:00Z","timestamp":1616457600000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1008623","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T18:02:12Z","timestamp":1616522532000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1008623"}},"subtitle":[],"editor":[{"given":"Dan S.","family":"Tawfik","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2021,3,8]]},"references-count":112,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,3,8]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1008623","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1008623","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,8]]}}}