Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
13 06 2022
13 06 2022
Historique:
received:
04
12
2021
accepted:
10
05
2022
entrez:
13
6
2022
pubmed:
14
6
2022
medline:
16
6
2022
Statut:
epublish
Résumé
The ESCRT machinery, comprising of multiple proteins and subcomplexes, is crucial for membrane remodelling in eukaryotic cells, in processes that include ubiquitin-mediated multivesicular body formation, membrane repair, cytokinetic abscission, and virus exit from host cells. This ESCRT system appears to have simpler, ancient origins, since many archaeal species possess homologues of ESCRT-III and Vps4, the components that execute the final membrane scission reaction, where they have been shown to play roles in cytokinesis, extracellular vesicle formation and viral egress. Remarkably, metagenome assemblies of Asgard archaea, the closest known living relatives of eukaryotes, were recently shown to encode homologues of the entire cascade involved in ubiquitin-mediated membrane remodelling, including ubiquitin itself, components of the ESCRT-I and ESCRT-II subcomplexes, and ESCRT-III and Vps4. Here, we explore the phylogeny, structure, and biochemistry of Asgard homologues of the ESCRT machinery and the associated ubiquitylation system. We provide evidence for the ESCRT-I and ESCRT-II subcomplexes being involved in ubiquitin-directed recruitment of ESCRT-III, as it is in eukaryotes. Taken together, our analyses suggest a pre-eukaryotic origin for the ubiquitin-coupled ESCRT system and a likely path of ESCRT evolution via a series of gene duplication and diversification events.
Identifiants
pubmed: 35697693
doi: 10.1038/s41467-022-30656-2
pii: 10.1038/s41467-022-30656-2
pmc: PMC9192718
doi:
Substances chimiques
Endosomal Sorting Complexes Required for Transport
0
Ubiquitin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3398Subventions
Organisme : Medical Research Council
ID : MC_U105184326
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203276/Z/16/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT101885MA
Pays : United Kingdom
Informations de copyright
© 2022. The Author(s).
Références
Henne, W. M., Buchkovich, N. J. & Emr, S. D. Developmental Cell Vol. 21 (Cell Press, 2011).
Piper, R. C., Cooper, A. A., Yang, H. & Stevens, T. H. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell Biol. 131, 603–617 (1995).
pubmed: 7593183
doi: 10.1083/jcb.131.3.603
Li, Y., Kane, T., Tipper, C., Spatrick, P. & Jenness, D. D. Yeast mutants affecting possible quality control of plasma membrane proteins. Mol. Cell. Biol. 19, 3588–3599 (1999).
pubmed: 10207082
pmcid: 84152
doi: 10.1128/MCB.19.5.3588
Rieder, S. E., Banta, L. M., Köhrer, K., McCaffery, J. M. & Emr, S. D. Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol. Biol. Cell 7, 985–999 (1996).
pubmed: 8817003
pmcid: 275948
doi: 10.1091/mbc.7.6.985
Babst, M., Odorizzi, G., Estepa, E. J. & Emr, S. D. Mammalian Tumor Susceptibility Gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal. Trafficking. Traffic 1, 248–258 (2000).
pubmed: 11208108
doi: 10.1034/j.1600-0854.2000.010307.x
Munn, A. L. & Riezman, H. Endocytosis is required for the growth of vacuolar H(+)-ATPase- defective yeast: identification of six new END genes. J. Cell Biol. 127, 373–386 (1994).
pubmed: 7929582
doi: 10.1083/jcb.127.2.373
Nothwehr, S. F., Bryant, N. J. & Stevens, T. H. The newly identified yeast GRD genes are required for retention of late-Golgi membrane proteins. Mol. Cell Biol. 16, 2700–7 (1996).
Babst, M., Sato, T. K., Banta, L. M. & Emr, S. D. Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16, 1820–1831 (1997).
pubmed: 9155008
pmcid: 1169785
doi: 10.1093/emboj/16.8.1820
Katzmann, D. J., Babst, M. & Emr, S. D. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145–155 (2001).
pubmed: 11511343
doi: 10.1016/S0092-8674(01)00434-2
Kranz, A., Kinner, A. & Kölling, R. A family of small coiled-coil–forming proteins functioning at the late endosome in yeast. Mol. Biol. Cell 12, 711–723 (2001).
pubmed: 11251082
pmcid: 30975
doi: 10.1091/mbc.12.3.711
Babst, M., Katzmann, D. J., Snyder, W. B., Wendland, B. & Emr, S. D. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Developmental cell 3, 283–289 (2002).
pubmed: 12194858
doi: 10.1016/S1534-5807(02)00219-8
Katzmann, D. J., Stefan, C. J., Babst, M. & Emr, S. D. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413–423 (2003).
pubmed: 12900393
pmcid: 2172707
doi: 10.1083/jcb.200302136
Bilodeau, P. S., Winistorfer, S. C., Kearney, W. R., Robertson, A. D. & Piper, R. C. Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163, 237–243 (2003).
pubmed: 14581452
pmcid: 2173515
doi: 10.1083/jcb.200305007
Shih, S. C. et al. Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4, 389–393 (2002).
pubmed: 11988742
doi: 10.1038/ncb790
Odorizzi, G., Babst, M. & Emr, S. D. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847–858 (1998).
pubmed: 9865702
doi: 10.1016/S0092-8674(00)81707-9
von Schwedler, U. K. et al. The protein network of HIV budding. Cell 114, 701–713 (2003).
doi: 10.1016/S0092-8674(03)00714-1
Strack, B., Calistri, A., Craig, S., Popova, E. & Göttlinger, H. G. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689–699 (2003).
pubmed: 14505569
doi: 10.1016/S0092-8674(03)00653-6
Martin-Serrano, J., Yarovoy, A., Perez-Caballero, D., Bieniasz, P. D. & Yaravoy, A. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl Acad. Sci. USA 100, 12414–12419 (2003).
pubmed: 14519844
pmcid: 218772
doi: 10.1073/pnas.2133846100
Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908–1912 (2007).
pubmed: 17556548
doi: 10.1126/science.1143422
Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215–4227 (2007).
pubmed: 17853893
pmcid: 2230844
doi: 10.1038/sj.emboj.7601850
VerPlank, L. et al. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55Gag. Proc. Natl Acad. Sci. USA 98, 7724–7729 (2001).
pubmed: 11427703
pmcid: 35409
doi: 10.1073/pnas.131059198
Martin-Serrano, J., Zang, T. & Bieniasz, P. D. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7, 1313–1319 (2001).
pubmed: 11726971
doi: 10.1038/nm1201-1313
Skowyra, M. L., Schlesinger, P. H., Naismith, T. V. & Hanson, P. I. Triggered recruitment of ESCRT machinery promotes endolysosomal repair. Science 360, eaar5078–eaar5078 (2018).
pubmed: 29622626
pmcid: 6195421
doi: 10.1126/science.aar5078
Jimenez, A. J. et al. ESCRT machinery is required for plasma membrane repair. Science 343, 1247136–1247136 (2014).
pubmed: 24482116
doi: 10.1126/science.1247136
Scheffer, L. L. et al. Mechanism of Ca
pubmed: 25534348
doi: 10.1038/ncomms6646
Choi, H. W. et al. Perivascular dendritic cells elicit anaphylaxis by relaying allergens to mast cells via microvesicles. Science 362, eaao0666 (2018).
pubmed: 30409859
pmcid: 6376486
doi: 10.1126/science.aao0666
Vietri, M. et al. Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522, 231–235 (2015).
pubmed: 26040712
doi: 10.1038/nature14408
Zhang, H. et al. Endocytic pathways downregulate the L1-type cell adhesion molecule neuroglian to promote dendrite pruning in drosophila. Developmental Cell 30, 463–478 (2014).
pubmed: 25158855
doi: 10.1016/j.devcel.2014.06.014
Loncle, N., Agromayor, M., Martin-Serrano, J. & Williams, D. W. An ESCRT module is required for neuron pruning. Sci. Rep. 5, 8461–8461 (2015).
pubmed: 25676218
pmcid: 4327575
doi: 10.1038/srep08461
Matusek, T. et al. The ESCRT machinery regulates the secretion and long-range activity of Hedgehog. Nature 516, 99–103 (2014).
pubmed: 25471885
doi: 10.1038/nature13847
Olmos, Y., Hodgson, L., Mantell, J., Verkade, P. & Carlton, J. G. ESCRT-III controls nuclear envelope reformation. Nature 522, 236–239 (2015).
pubmed: 26040713
pmcid: 4471131
doi: 10.1038/nature14503
Denais, C. M. et al. Nuclear envelope rupture and repair during cancer cell migration. Science 352, 353–358 (2016).
pubmed: 27013428
pmcid: 4833568
doi: 10.1126/science.aad7297
Raab, M. et al. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352, 359–362 (2016).
pubmed: 27013426
doi: 10.1126/science.aad7611
Frost, A. et al. Functional repurposing revealed by comparing S. pombe and S. cerevisiae genetic interactions. Cell 149, 1339–1352 (2012).
pubmed: 22682253
pmcid: 3613983
doi: 10.1016/j.cell.2012.04.028
Webster, B. M., Colombi, P., Jäger, J. & Patrick Lusk, C. Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159, 388–401 (2014).
pubmed: 25303532
pmcid: 4194032
doi: 10.1016/j.cell.2014.09.012
Zhou, F. et al. Rab5-dependent autophagosome closure by ESCRT. J. Cell Biol. 218, 1908–1927 (2019).
pubmed: 31010855
pmcid: 6548130
doi: 10.1083/jcb.201811173
Takahashi, Y. et al. An autophagy assay reveals the ESCRT-III component CHMP2A as a regulator of phagophore closure. Nat. Commun. 9, 1–13 (2018).
doi: 10.1038/s41467-018-05254-w
Sahu, R. et al. Microautophagy of cytosolic proteins by late endosomes. Developmental Cell 20, 131–139 (2011).
pubmed: 21238931
pmcid: 3025279
doi: 10.1016/j.devcel.2010.12.003
Radulovic, M. et al. ESCRT-mediated lysosome repair precedes lysophagy and promotes cell survival. EMBO J. 37, e99753 (2018).
pubmed: 30314966
pmcid: 6213280
doi: 10.15252/embj.201899753
Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature Vol. 458, 445–452 (Nature Publishing Group, 2009).
Raiborg, C. et al. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4, 394–398 (2002).
pubmed: 11988743
doi: 10.1038/ncb791
Bilodeau, P. S., Urbanowski, J. L., Winistorfer, S. C. & Piper, R. C. The Vps27p–Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4, 534–539 (2002).
pubmed: 12055639
doi: 10.1038/ncb815
Babst, M., Wendland, B., Estepa, E. J. & Emr, S. D. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982–2993 (1998).
pubmed: 9606181
pmcid: 1170638
doi: 10.1093/emboj/17.11.2982
Babst, M., Katzmann, D. J., Estepa-Sabal, E. J., Meerloo, T. & Emr, S. D. ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Developmental Cell 3, 271–282 (2002).
pubmed: 12194857
doi: 10.1016/S1534-5807(02)00220-4
Hanson, P. I., Roth, R., Lin, Y. & Heuser, J. E. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389–402 (2008).
pubmed: 18209100
pmcid: 2213594
doi: 10.1083/jcb.200707031
Teis, D., Saksena, S. & Emr, S. D. Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Developmental Cell 15, 578–589 (2008).
pubmed: 18854142
doi: 10.1016/j.devcel.2008.08.013
Lata, S. et al. Helical structures of ESCRT-III are disassembled by VPS4. Science 321, 1354–1357 (2008).
pubmed: 18687924
pmcid: 2758909
doi: 10.1126/science.1161070
Chiaruttini, N. et al. Relaxation of loaded ESCRT-III spiral springs drives membrane deformation. Cell 163, 866–879 (2015).
pubmed: 26522593
pmcid: 4644223
doi: 10.1016/j.cell.2015.10.017
Mierzwa, B. E. et al. Dynamic subunit turnover in ESCRT-III assemblies is regulated by Vps4 to mediate membrane remodelling during cytokinesis. Nat. Cell Biol. 19, 787–798 (2017).
pubmed: 28604678
pmcid: 5493987
doi: 10.1038/ncb3559
Maity, S. et al. VPS4 triggers constriction and cleavage of ESCRT-III helical filaments. Sci. Adv. 5, eaau7198 (2019).
pubmed: 30989108
pmcid: 6457934
doi: 10.1126/sciadv.aau7198
Teis, D., Saksena, S., Judson, B. L. & Emr, S. D. ESCRT-II coordinates the assembly of ESCRT-III filaments for cargo sorting and multivesicular body vesicle formation. EMBO J. 29, 871–883 (2010).
pubmed: 20134403
pmcid: 2837172
doi: 10.1038/emboj.2009.408
Saksena, S., Wahlman, J., Teis, D., Johnson, A. E. & Emr, S. D. Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136, 97–109 (2009).
pubmed: 19135892
pmcid: 4104304
doi: 10.1016/j.cell.2008.11.013
Pfitzner, A. K. et al. An ESCRT-III polymerization sequence drives membrane deformation and fission. Cell 182, 1140–1155.e1118 (2020).
pubmed: 32814015
pmcid: 7479521
doi: 10.1016/j.cell.2020.07.021
Leung, K. F., Dacks, J. B. & Field, M. C. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698–1716 (2008).
pubmed: 18637903
doi: 10.1111/j.1600-0854.2008.00797.x
Obita, T. et al. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735–739 (2007).
pubmed: 17928861
doi: 10.1038/nature06171
Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L. & Bell, S. D. A role for the ESCRT system in cell division in archaea. Science 322, 1710–1713 (2008).
pubmed: 19008417
pmcid: 4121953
doi: 10.1126/science.1165322
Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).
pubmed: 25945739
pmcid: 4444528
doi: 10.1038/nature14447
Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature https://doi.org/10.1038/nature21031 (2017).
Lindås, A.-C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. G. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci. USA 105, 18942–18946 (2008).
pubmed: 18987308
pmcid: 2596248
doi: 10.1073/pnas.0809467105
Snyder, J. C., Samson, R. Y., Brumfield, S. K., Bell, S. D. & Young, M. J. Functional interplay between a virus and the ESCRT machinery in Archaea. Proc. Natl Acad. Sci. USA 110, 10783–10787 (2013).
pubmed: 23754419
pmcid: 3696792
doi: 10.1073/pnas.1301605110
Lu, Z. et al. Coevolution of eukaryote-like Vps4 and ESCRT-III subunits in the asgard archaea. mBio, 11, e00417-20 https://doi.org/10.1128/mBio.00417-20 (2020).
Gupta, T. K. et al. Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity. Cell 184, 3643–3659 e3623 (2021).
pubmed: 34166613
doi: 10.1016/j.cell.2021.05.011
Junglas, B. et al. PspA adopts an ESCRT-III-like fold and remodels bacterial membranes. Cell 184, 3674–3688 e3618 (2021).
pubmed: 34166616
doi: 10.1016/j.cell.2021.05.042
Liu, J. et al. Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. Cell 184, 3660–3673 e3618 (2021).
pubmed: 34166615
pmcid: 8281802
doi: 10.1016/j.cell.2021.05.041
Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011).
pubmed: 21169198
doi: 10.1093/nar/gkq1228
Hennell James, R. et al. Functional reconstruction of a eukaryotic-like E1/E2/(RING) E3 ubiquitylation cascade from an uncultured archaeon. Nat. Commun. 8, 1–15 https://doi.org/10.1038/s41467-017-01162-7 (2017).
Imachi, H. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577, 519–525 (2020).
pubmed: 31942073
pmcid: 7015854
doi: 10.1038/s41586-019-1916-6
Seitz, K. W. et al. Asgard archaea capable of anaerobic hydrocarbon cycling. Nat. Commun. 10, 1–11 (2019).
doi: 10.1038/s41467-019-09364-x
Tamarit, D. et al. A closed Odinarchaeum genome exposes Asgard archaeal viruses. Nature Microbiology. In Press (2022). bioRxiv https://doi.org/10.1101/2021.09.01.458545 .
Stuchell, M. D. et al. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J. Biol. Chem. 279, 36059–36071 (2004).
pubmed: 15218037
doi: 10.1074/jbc.M405226200
Bache, K. G. et al. The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol. Biol. Cell 15, 4337–4346 (2004).
pubmed: 15240819
pmcid: 515363
doi: 10.1091/mbc.e04-03-0250
Kostelansky, M. S. et al. Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129, 485–498 (2007).
pubmed: 17442384
pmcid: 2065850
doi: 10.1016/j.cell.2007.03.016
Sancho, E. et al. Role of UEV-1, an inactive variant of the E2 ubiquitin conjugating enzymes, in in vitro differentiation and cell cycle behavior of HT-29-M6 intestinal mucosecretory cells. Mol. Cell. Biol. 18, 576–589 (1998).
pubmed: 9418904
pmcid: 121525
doi: 10.1128/MCB.18.1.576
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat Methods 19, 679–682 https://doi.org/10.1038/s41592-022-01488-1 (2022).
Teo, H. et al. ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125, 99–111 (2006).
pubmed: 16615893
doi: 10.1016/j.cell.2006.01.047
Boura, E. et al. Solution structure of the ESCRT-I and -II supercomplex: implications for membrane budding and scission. Struct. (Lond., Engl.: 1993) 20, 874–886 (2012).
doi: 10.1016/j.str.2012.03.008
Flower, T. G. et al. A helical assembly of human ESCRT-I scaffolds reverse-topology membrane scission. Nat. Struct. Mol. Biol. 27, 570–580 (2020).
pubmed: 32424346
pmcid: 7339825
doi: 10.1038/s41594-020-0426-4
Hierro, A. et al. Structure of the ESCRT-II endosomal trafficking complex. Nature 431, 221–225 (2004).
pubmed: 15329733
doi: 10.1038/nature02914
Teo, H., Perisic, O., González, B. & Williams, R. L. ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7, 559–569 (2004).
pubmed: 15469844
doi: 10.1016/j.devcel.2004.09.003
Im, Y. J. & Hurley, J. H. Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev. Cell 14, 902–913 (2008).
pubmed: 18539118
pmcid: 2475506
doi: 10.1016/j.devcel.2008.04.004
Wernimont, A. K. & Weissenhorn, W. Crystal structure of subunit VPS25 of the endosomal trafficking complex ESCRT-II. BMC Struct. Biol. 4, 10 (2004).
pubmed: 15579210
pmcid: 539351
doi: 10.1186/1472-6807-4-10
Schrödinger, L. a. W. D. The PyMOL Molecular Graphics System. http://www.pymol.org/pymol (2020).
Bornberg-Bauer, E. & Albà, M. M. Dynamics and adaptive benefits of modular protein evolution. Curr Opin Struct Biol. 23, 459–466. https://doi.org/10.1016/j.sbi.2013.02.012 (2013).
Copley, S. D. Evolution of new enzymes by gene duplication and divergence. FEBS J. 287, 1262–1283 (2020).
pubmed: 32250558
doi: 10.1111/febs.15299
Hong Feng, G., Lih, C.-J. & Cohen, S. N. TSG101 protein steady-state level is regulated posttranslationally by an evolutionarily conserved COOH-terminal sequence. Cancer Res. 60, 1736–1741 (2000).
Imachi, H. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577, 519–525 (2020).
pubmed: 31942073
pmcid: 7015854
doi: 10.1038/s41586-019-1916-6
Heimerl, T. et al. A complex endomembrane system in the archaeon ignicoccus hospitalis tapped by nanoarchaeum equitans. Front. Microbiol. 8, 1072 (2017).
pubmed: 28659892
pmcid: 5468417
doi: 10.3389/fmicb.2017.01072
Liu, J. et al. Archaeal extracellular vesicles are produced in an ESCRT-dependent manner and promote gene transfer and nutrient cycling in extreme environments. ISME J. 15, 2892–2905 (2021).
pubmed: 33903726
doi: 10.1038/s41396-021-00984-0
Snyder, J. C. & Young, M. J. Potential role of cellular ESCRT proteins in the STIV life cycle. Biochemical Soc. Trans. 39, 107–110 (2011).
doi: 10.1042/BST0390107
Lindas, A. C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci. USA 105, 18942–18946 (2008).
pubmed: 18987308
pmcid: 2596248
doi: 10.1073/pnas.0809467105
Snyder, J. C., Samson, R. Y., Brumfield, S. K., Bell, S. D. & Young, M. J. Functional interplay between a virus and the ESCRT machinery in archaea. Proc. Natl Acad. Sci. USA 110, 10783–10787 (2013).
pubmed: 23754419
pmcid: 3696792
doi: 10.1073/pnas.1301605110
Ellen, A. F. et al. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13, 67–79 (2009).
pubmed: 18972064
doi: 10.1007/s00792-008-0199-x
Dobro, M. J. et al. Electron cryotomography of ESCRT assemblies and dividing Sulfolobus cells suggests that spiraling filaments are involved in membrane scission. Mol. Biol. Cell 24, 2319–2327 (2013).
pubmed: 23761076
pmcid: 3727925
doi: 10.1091/mbc.e12-11-0785
Samson, R. Y. et al. Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol. Cell 41, 186–196 (2011).
pubmed: 21255729
pmcid: 3763469
doi: 10.1016/j.molcel.2010.12.018
Liu, J. et al. Functional assignment of multiple ESCRT-III homologs in cell division and budding in Sulfolobus islandicus. Mol. Microbiol. 105, 540–553 (2017).
pubmed: 28557139
doi: 10.1111/mmi.13716
Baum, D. A. & Baum, B. An inside-out origin for the eukaryotic cell. BMC Biol. 12, 76 (2014).
pubmed: 25350791
pmcid: 4210606
doi: 10.1186/s12915-014-0076-2
Hug, L. A. et al. Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1, 22 (2013).
pubmed: 24450983
pmcid: 3971608
doi: 10.1186/2049-2618-1-22
Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma. 11, 119 (2010).
doi: 10.1186/1471-2105-11-119
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
pubmed: 9254694
pmcid: 146917
doi: 10.1093/nar/25.17.3389
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
pubmed: 19505945
pmcid: 2712344
doi: 10.1093/bioinformatics/btp348
Minh, B. Q. et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
pubmed: 32011700
pmcid: 7182206
doi: 10.1093/molbev/msaa015
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).
pubmed: 29077904
doi: 10.1093/molbev/msx281
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2018).
Wickham, H. Use R! (Springer International Publishing, 2016).
cowplot. cowplot: Streamlined Plot Theme and Plot Annotations for ‘ggplot2’. v. R Package Version 1.0.0. (cowplot, 2019).
Guy, L., Kultima, J. R. & Andersson, S. G. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26, 2334–2335 (2010).
pubmed: 20624783
pmcid: 2935412
doi: 10.1093/bioinformatics/btq413
Im, Y. J., Wollert, T., Boura, E. & Hurley, J. H. Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Dev. Cell 17, 234–243 (2009).
pubmed: 19686684
pmcid: 2749878
doi: 10.1016/j.devcel.2009.07.008
Gill, D. J. et al. Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J. 26, 600–612 (2007).
pubmed: 17215868
pmcid: 1783442
doi: 10.1038/sj.emboj.7601501
VanDemark, A. P., Hofmann, R. M., Tsui, C., Pickart, C. M. & Wolberger, C. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105, 711–720 (2001).
pubmed: 11440714
doi: 10.1016/S0092-8674(01)00387-7
Teo, H., Veprintsev, D. B. & Williams, R. L. Structural insights into endosomal sorting complex required for transport (ESCRT-I) recognition of ubiquitinated proteins. J. Biol. Chem. 279, 28689–28696 (2004).
pubmed: 15044434
doi: 10.1074/jbc.M400023200
Baker, B. J. et al. Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea. Nat. Microbiol 1, 16002 (2016).
pubmed: 27572167
doi: 10.1038/nmicrobiol.2016.2
Geissler, S. et al. The spindle pole body component Spc98p interacts with the gamma-tubulin-like Tub4p of Saccharomyces cerevisiae at the sites of microtubule attachment. EMBO J. 15, 3899–3911 (1996).
pubmed: 8670895
pmcid: 452092
doi: 10.1002/j.1460-2075.1996.tb00764.x
Gyuris, J., Golemis, E., Chettkov, H. & Brent, R. Cdil, a Human Gl and S Phase Protein Phosphatase That Associates with Cdk2. Cell 75, 791–803 (1993).
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Lemoine, F. et al. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556, 452–456 (2018).
pubmed: 29670290
pmcid: 6030568
doi: 10.1038/s41586-018-0043-0
Wang, H. C., Minh, B. Q., Susko, E. & Roger, A. J. Modeling site heterogeneity with posterior mean site frequency profiles accelerates accurate phylogenomic estimation. Syst. Biol. 67, 216–235 (2018).
pubmed: 28950365
doi: 10.1093/sysbio/syx068
Frey, S. & Görlich, D. A new set of highly efficient, tag-cleaving proteases for purifying recombinant proteins. J. Chromatogr. A 1337, 95–105 (2014).
pubmed: 24636565
doi: 10.1016/j.chroma.2014.02.029
Liu, L., Spurrier, J., Butt, T. R. & Strickler, J. E. Enhanced protein expression in the baculovirus/insect cell system using engineered SUMO fusions. Protein Expr. Purif. 62, 21–28 (2008).
pubmed: 18713650
pmcid: 2585507
doi: 10.1016/j.pep.2008.07.010
Micsonai, A. et al. BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucleic Acids Res. 46, W315–W322 (2018).
pubmed: 29893907
pmcid: 6031044
doi: 10.1093/nar/gky497
Frishman, D. & Argos, P. Knowledge-based protein secondary structure assignment. Proteins 23, 566–579 (1995).
pubmed: 8749853
doi: 10.1002/prot.340230412
Stock, D., Perisic, O. & Lowe, J. Robotic nanolitre protein crystallisation at the MRC Laboratory of Molecular Biology. Prog. Biophys. Mol. Biol. 88, 311–327 (2005).
pubmed: 15652247
doi: 10.1016/j.pbiomolbio.2004.07.009
Gorrec, F. The MORPHEUS protein crystallization screen. J. Appl. Crystallogr. 42, 1035–1042 (2009).
pubmed: 22477774
pmcid: 3246824
doi: 10.1107/S0021889809042022
Winter, G. et al. DIALS: implementation and evaluation of a new integration package. Acta Crystallogr D. Struct. Biol. 74, 85–97 (2018).
pubmed: 29533234
pmcid: 5947772
doi: 10.1107/S2059798317017235
Evans, P. R. M. G. N. How good are my data and what is the resolution? Acta Crystallogr. Sect. D: Biol. Crystallogr. 69, 1204–1214 (2013).
doi: 10.1107/S0907444913000061
Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D. Biol. Crystallogr 67, 235–242 (2011).
pubmed: 21460441
pmcid: 3069738
doi: 10.1107/S0907444910045749
Long, F., Vagin, A. A., Young, P. & Murshudov, G. N. BALBES: a molecular-replacement pipeline Acta Crystallographica Section D: Biological Crystallography (International Union of Crystallography, 2008) 64, 125-132 (2008).
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. Sect. D: Biol. Crystallogr. 66, 486–501 (2010).
doi: 10.1107/S0907444910007493
Chen, V. B. et al. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr. Sect. D: Biol. Crystallogr. 66, 12–21 (2010).
doi: 10.1107/S0907444909042073
Holman, J. D., Tabb, D. L. & Mallick, P. Employing ProteoWizard to Convert Raw Mass Spectrometry Data. Current Protocols in Bioinformatics, 46, 13.24.1-13.24.9 https://doi.org/10.1002/0471250953.bi1324s46 (2014).
Götze, M. et al. StavroX-A software for analyzing crosslinked products in protein interaction studies. J. Am. Soc. Mass Spectrom. 23, 76–87 (2012).
pubmed: 22038510
doi: 10.1007/s13361-011-0261-2
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2