Identification and structure of an extracellular contractile injection system from the marine bacterium Algoriphagus machipongonensis.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
received:
26
10
2021
accepted:
05
01
2022
pubmed:
16
2
2022
medline:
7
4
2022
entrez:
15
2
2022
Statut:
ppublish
Résumé
Contractile injection systems (CISs) are phage tail-like nanomachines, mediating bacterial cell-cell interactions as either type VI secretion systems (T6SSs) or extracellular CISs (eCISs). Bioinformatic studies uncovered a phylogenetic group of hundreds of putative CIS gene clusters that are highly diverse and widespread; however, only four systems have been characterized. Here we studied a putative CIS gene cluster in the marine bacterium Algoriphagus machipongonensis. Using an integrative approach, we show that the system is compatible with an eCIS mode of action. Our cryo-electron microscopy structure revealed several features that differ from those seen in other CISs: a 'cap adaptor' located at the distal end, a 'plug' exposed to the tube lumen, and a 'cage' formed by massive extensions of the baseplate. These elements are conserved in other CISs, and our genetic tools identified that they are required for assembly, cargo loading and function. Furthermore, our atomic model highlights specific evolutionary hotspots and will serve as a framework for understanding and re-engineering CISs.
Identifiants
pubmed: 35165385
doi: 10.1038/s41564-022-01059-2
pii: 10.1038/s41564-022-01059-2
pmc: PMC8894135
doi:
Substances chimiques
Type VI Secretion Systems
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
397-410Subventions
Organisme : Howard Hughes Medical Institute
Pays : United States
Commentaires et corrections
Type : CommentIn
Type : ErratumIn
Informations de copyright
© 2022. The Author(s).
Références
Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010).
pubmed: 19946288
pmcid: 2879262
doi: 10.1038/nrmicro2259
Kooger, R., Szwedziak, P., Böck, D. & Pilhofer, M. CryoEM of bacterial secretion systems. Curr. Opin. Struct. Biol. 52, 64–70 (2018).
pubmed: 30223223
doi: 10.1016/j.sbi.2018.08.007
Galán, J. E. & Waksman, G. Protein-injection machines in bacteria. Cell 172, 1306–1318 (2018).
pubmed: 29522749
pmcid: 5849082
doi: 10.1016/j.cell.2018.01.034
Costa, T. R. D. et al. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13, 343–359 (2015).
pubmed: 25978706
doi: 10.1038/nrmicro3456
Veesler, D. & Cambillau, C. A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol. Mol. Biol. Rev. 75, 423–433 (2011).
pubmed: 21885679
pmcid: 3165541
doi: 10.1128/MMBR.00014-11
Leiman, P. G. et al. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl Acad. Sci. USA 106, 4154–4159 (2009).
pubmed: 19251641
pmcid: 2657435
doi: 10.1073/pnas.0813360106
Brackmann, M., Nazarov, S., Wang, J. & Basler, M. Using force to punch holes: mechanics of contractile nanomachines. Trends Cell Biol. 27, 623–632 (2017).
pubmed: 28602424
doi: 10.1016/j.tcb.2017.05.003
Leiman, P. G. & Shneider, M. M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 726, 93–114 (2012).
pubmed: 22297511
doi: 10.1007/978-1-4614-0980-9_5
Dams, D., Brøndsted, L., Drulis-Kawa, Z. & Briers, Y. Engineering of receptor-binding proteins in bacteriophages and phage tail-like bacteriocins. Biochem. Soc. Trans. 47, 449–460 (2019).
pubmed: 30783013
doi: 10.1042/BST20180172
Taylor, N. M. I., van Raaij, M. J. & Leiman, P. G. Contractile injection systems of bacteriophages and related systems. Mol. Microbiol. 108, 6–15 (2018).
pubmed: 29405518
doi: 10.1111/mmi.13921
Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J. & Mekalanos, J. J. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483, 182–186 (2012).
pubmed: 22367545
pmcid: 3527127
doi: 10.1038/nature10846
Nazarov, S. et al. Cryo‐EM reconstruction of Type VI secretion system baseplate and sheath distal end. EMBO J. 37, e201797103 (2017).
Nguyen, V. S. et al. Towards a complete structural deciphering of Type VI secretion system. Curr. Opin. Struct. Biol. 49, 77–84 (2018).
pubmed: 29414515
doi: 10.1016/j.sbi.2018.01.007
Durand, E. et al. Biogenesis and structure of a type VI secretion membrane core complex. Nature 523, 555–560 (2015).
pubmed: 26200339
doi: 10.1038/nature14667
Basler, M., Ho, B. T. & Mekalanos, J. J. Tit-for-tat: type VI secretion system counterattack during bacterial cell–cell interactions. Cell 152, 884–894 (2013).
pubmed: 23415234
pmcid: 3616380
doi: 10.1016/j.cell.2013.01.042
Böck, D. et al. In situ architecture, function, and evolution of a contractile injection system. Science 357, 713–717 (2017).
pubmed: 28818949
pmcid: 6485382
doi: 10.1126/science.aan7904
Chen, L. et al. Genome-wide identification and characterization of a superfamily of bacterial extracellular contractile injection systems. Cell Rep. 29, 511–521.e2 (2019).
pubmed: 31597107
pmcid: 6899500
doi: 10.1016/j.celrep.2019.08.096
Sarris, P. F., Ladoukakis, E. D., Panopoulos, N. J. & Scoulica, E. V. A phage tail-derived element with wide distribution among both prokaryotic domains: a comparative genomic and phylogenetic study. Genome Biol. Evol. 6, 1739–1747 (2014).
pubmed: 25015235
pmcid: 4122934
doi: 10.1093/gbe/evu136
Geller, A. M. et al. The extracellular contractile injection system is enriched in environmental microbes and associates with numerous toxins. Nat. Commun. 12, 3743 (2021).
pubmed: 34145238
pmcid: 8213781
doi: 10.1038/s41467-021-23777-7
Yang, G., Dowling, A. J., Gerike, U., ffrench-Constant, R. H. & Waterfield, N. R. Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth. J. Bacteriol. 188, 2254–2261 (2006).
pubmed: 16513755
pmcid: 1428146
doi: 10.1128/JB.188.6.2254-2261.2006
Hurst, M. R. H., Glare, T. R. & Jackson, T. A. Cloning Serratia entomophila antifeeding genes—a putative defective prophage active against the grass grub Costelytra zealandica. J. Bacteriol. 186, 5116–5128 (2004).
pubmed: 15262948
pmcid: 451664
doi: 10.1128/JB.186.15.5116-5128.2004
Shikuma, N. J. et al. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343, 529–533 (2014).
pubmed: 24407482
pmcid: 4949041
doi: 10.1126/science.1246794
Rocchi, I. et al. A bacterial phage tail-like structure kills eukaryotic cells by injecting a nuclease effector. Cell Rep. 28, 295–301.e4 (2019).
pubmed: 31291567
doi: 10.1016/j.celrep.2019.06.019
Jiang, F. et al. Cryo-EM structure and assembly of an extracellular contractile injection system. Cell 177, 370–383.e15 (2019).
pubmed: 30905475
doi: 10.1016/j.cell.2019.02.020
Desfosses, A. et al. Atomic structures of an entire contractile injection system in both the extended and contracted states. Nat. Microbiol. 4, 1885–1894 (2019).
pubmed: 31384001
pmcid: 6817355
doi: 10.1038/s41564-019-0530-6
Alegado, R. A. et al. Algoriphagus machipongonensis sp. nov., co-isolated with a colonial choanoflagellate. Int. J. Syst. Evol. Microbiol. 63, 163–168 (2013).
pubmed: 22368173
pmcid: 3709532
doi: 10.1099/ijs.0.038646-0
Alegado, R. A. et al. A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1, e00013 (2012).
pubmed: 23066504
pmcid: 3463246
doi: 10.7554/eLife.00013
Woznica, A. et al. Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc. Natl Acad. Sci. USA 113, 7894–7899 (2016).
pubmed: 27354530
pmcid: 4948368
doi: 10.1073/pnas.1605015113
Cantley, A. M., Woznica, A., Beemelmanns, C., King, N. & Clardy, J. Isolation and synthesis of a bacterially produced inhibitor of rosette development in choanoflagellates. J. Am. Chem. Soc. 138, 4326–4329 (2016).
pubmed: 26998963
pmcid: 4968929
doi: 10.1021/jacs.6b01190
Ge, P. et al. Action of a minimal contractile bactericidal nanomachine. Nature https://doi.org/10.1038/s41586-020-2186-z (2020).
Kino, Y. et al. Counterselection employing mutated pheS for markerless genetic deletion in Bacteroides species. Anaerobe 42, 81–88 (2016).
pubmed: 27639596
doi: 10.1016/j.anaerobe.2016.09.004
Miyazaki, K. Molecular engineering of a PheS counterselection marker for improved operating efficiency in Escherichia coli. Biotechniques 58, 86–88 (2015).
pubmed: 25652032
doi: 10.2144/000114257
Rybakova, D. et al. Role of antifeeding prophage (Afp) protein Afp16 in terminating the length of the Afp tailocin and stabilizing its sheath. Mol. Microbiol. 89, 702–714 (2013).
pubmed: 23796263
doi: 10.1111/mmi.12305
Zheng, W. et al. Refined Cryo-EM structure of the T4 tail tube: exploring the lowest dose limit. Structure 25, 1436–1441.e2 (2017).
pubmed: 28757144
pmcid: 5587399
doi: 10.1016/j.str.2017.06.017
Kanamaru, S. et al. Structure of the cell-puncturing device of bacteriophage T4. Nature 415, 553–557 (2002).
pubmed: 11823865
doi: 10.1038/415553a
Ericson, C. F. et al. A contractile injection system stimulates tubeworm metamorphosis by translocating a proteinaceous effector. eLife 8, e46845 (2019).
pubmed: 31526475
pmcid: 6748791
doi: 10.7554/eLife.46845
Taylor, N. M. I. et al. Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 533, 346–352 (2016).
pubmed: 27193680
doi: 10.1038/nature17971
Holm, L. DALI and the persistence of protein shape. Protein Sci. 29, 128–140 (2020).
pubmed: 31606894
doi: 10.1002/pro.3749
Boraston, A. B., Revett, T. J., Boraston, C. M., Nurizzo, D. & Davies, G. J. Structural and thermodynamic dissection of specific mannan recognition by a carbohydrate binding module, TmCBM27. Structure 11, 665–675 (2003).
pubmed: 12791255
doi: 10.1016/S0969-2126(03)00100-X
Kudryashev, M. et al. Structure of the Type VI secretion system contractile sheath. Cell 160, 952–962 (2015).
pubmed: 25723169
pmcid: 4359589
doi: 10.1016/j.cell.2015.01.037
Kube, S. et al. Structure of the VipA/B Type VI secretion complex suggests a contraction-state-specific recycling mechanism. Cell Rep. 8, 20–30 (2014).
pubmed: 24953649
doi: 10.1016/j.celrep.2014.05.034
Nguyen, V. S. et al. Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex. Nat. Microbiol. 2, 17103 (2017).
pubmed: 28650463
doi: 10.1038/nmicrobiol.2017.103
Wood, T. E. et al. The Pseudomonas aeruginosa T6SS delivers a periplasmic toxin that disrupts bacterial cell morphology. Cell Rep. 29, 187–201.e7 (2019).
pubmed: 31577948
pmcid: 6899460
doi: 10.1016/j.celrep.2019.08.094
Williams, S. R., Gebhart, D., Martin, D. W. & Scholl, D. Retargeting R-type pyocins to generate novel bactericidal protein complexes. Appl. Environ. Microbiol. 74, 3868–3876 (2008).
pubmed: 18441117
pmcid: 2446544
doi: 10.1128/AEM.00141-08
Salazar, A. J., Sherekar, M., Tsai, J. & Sacchettini, J. C. R pyocin tail fiber structure reveals a receptor-binding domain with a lectin fold. PLoS ONE 14, e0211432 (2019).
pubmed: 30721244
pmcid: 6363177
doi: 10.1371/journal.pone.0211432
Vlisidou, I. et al. The Photorhabdus asymbiotica virulence cassettes deliver protein effectors directly into target eukaryotic cells. eLife 8, e46259 (2019).
pubmed: 31526474
pmcid: 6748792
doi: 10.7554/eLife.46259
Jank, T. et al. Tyrosine glycosylation of Rho by Yersinia toxin impairs blastomere cell behaviour in zebrafish embryos. Nat. Commun. 6, 7807 (2015).
pubmed: 26190758
doi: 10.1038/ncomms8807
Alegado, R. A. et al. Complete genome sequence of Algoriphagus sp. PR1, bacterial prey of a colony-forming choanoflagellate. J. Bacteriol. 193, 1485–1486 (2011).
pubmed: 21183675
doi: 10.1128/JB.01421-10
Weiss, G. L. et al. Structure of a thylakoid-anchored contractile injection system in multicellular cyanobacteria. Nat. Microbiol. https://doi.org/10.1038/s41564-021-01055-y (2022).
Ge, P. et al. Atomic structures of a bactericidal contractile nanotube in its pre- and postcontraction states. Nat. Struct. Mol. Biol. 22, 377–382 (2015).
pubmed: 25822993
pmcid: 4445970
doi: 10.1038/nsmb.2995
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
pubmed: 16182563
doi: 10.1016/j.jsb.2005.07.007
Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71–76 (1996).
pubmed: 8742726
doi: 10.1006/jsbi.1996.0013
Tegunov, D. & Cramer, P. Real-time cryo-electron microscopy data preprocessing with Warp. Nat. Methods 16, 1146–1152 (2019).
pubmed: 31591575
pmcid: 6858868
doi: 10.1038/s41592-019-0580-y
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
pubmed: 26592709
pmcid: 4711343
doi: 10.1016/j.jsb.2015.11.003
Castaño-Díez, D., Kudryashev, M., Arheit, M. & Stahlberg, H. Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J. Struct. Biol. 178, 139–151 (2012).
pubmed: 22245546
doi: 10.1016/j.jsb.2011.12.017
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 5494038
doi: 10.1038/nmeth.4193
Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. eLife 7, e42166 (2018).
pubmed: 30412051
pmcid: 6250425
doi: 10.7554/eLife.42166
He, S. & Scheres, S. H. W. Helical reconstruction in RELION. J. Struct. Biol. 198, 163–176 (2017).
pubmed: 28193500
pmcid: 5479445
doi: 10.1016/j.jsb.2017.02.003
Ilca, S. L. et al. Multiple liquid crystalline geometries of highly compacted nucleic acid in a dsRNA virus. Nature 570, 252–256 (2019).
pubmed: 31142835
doi: 10.1038/s41586-019-1229-9
Rosenthal, P. B. & Henderson, R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721–745 (2003).
pubmed: 14568533
doi: 10.1016/j.jmb.2003.07.013
Pettersen, E. F. et al. UCSF chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493
Song, Y. et al. High-resolution comparative modeling with RosettaCM. Structure 21, 1735–1742 (2013).
pubmed: 24035711
doi: 10.1016/j.str.2013.08.005
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925
Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).
pubmed: 28710774
doi: 10.1002/pro.3235
Zhu, Y. et al. Genetic analyses unravel the crucial role of a horizontally acquired alginate lyase for brown algal biomass degradation by Zobellia galactanivorans. Environ. Microbiol. 19, 2164–2181 (2017).
pubmed: 28205313
doi: 10.1111/1462-2920.13699
Delavat, F., Bidault, A., Pichereau, V. & Paillard, C. Rapid and efficient protocol to introduce exogenous DNA in Vibrio harveyi and Pseudoalteromonas sp. J. Microbiol. Methods 154, 1–5 (2018).
pubmed: 30287352
doi: 10.1016/j.mimet.2018.09.022
Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
pubmed: 15318951
pmcid: 517706
doi: 10.1186/1471-2105-5-113
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 390337
doi: 10.1093/nar/gkh340
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
pubmed: 29722887
pmcid: 5967553
doi: 10.1093/molbev/msy096
Karimova, G., Ullmann, A. & Ladant, D. A bacterial two-hybrid system that exploits a cAMP signaling cascade in Escherichia coli. Methods Enzymol. 328, 59–73 (2000).
pubmed: 11075338
doi: 10.1016/S0076-6879(00)28390-0
Schaefer, J., Jovanovic, G., Kotta-Loizou, I. & Buck, M. A data comparison between a traditional and the single-step β-galactosidase assay. Data Brief 8, 350–352 (2016).
pubmed: 27331113
pmcid: 4908277
doi: 10.1016/j.dib.2016.05.063
Miller, J. H. Experiments in Molecular Genetics (Cold Spring Harbor Laboratory, 1972).
Booth, D. S. & King, N. Genome editing enables reverse genetics of multicellular development in the choanoflagellate Salpingoeca rosetta. eLife 9, e56193 (2020).
pubmed: 32496191
pmcid: 7314544
doi: 10.7554/eLife.56193
Booth, D. S., Szmidt-Middleton, H. & King, N. Choanoflagellate transfection illuminates their cell biology and the ancestry of animal septins. Mol. Biol. Cell 29, mbcE18080514 (2018).
doi: 10.1091/mbc.E18-08-0514
Levin, T. C., Greaney, A. J., Wetzel, L. & King, N. The rosetteless gene controls development in the choanoflagellate S. rosetta. eLife 3, e04070 (2014).
pmcid: 4381721
doi: 10.7554/eLife.04070
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Robert, X. & Gouet, P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42, W320–W324 (2014).
pubmed: 24753421
pmcid: 4086106
doi: 10.1093/nar/gku316
Shinya, S. et al. Mechanism of chitosan recognition by CBM32 carbohydrate-binding modules from a Paenibacillus sp. IK-5 chitosanase/glucanase. Biochem. J. 473, 1085–1095 (2016).
pubmed: 26936968
doi: 10.1042/BCJ20160045