DOI: 10.1146/annurev-micro-090817-062702. Using Cryo-EM to Investigate Bacterial Secretion Systems

Using Cryo-EM to Investigate Bacterial Secretion Systems

10.1146/annurev-micro-090817-062702

Crossref journal-article

Annual Reviews

Annual Review of Microbiology (22)

Abstract

Bacterial secretion systems are responsible for releasing macromolecules to the extracellular milieu or directly into other cells. These membrane complexes are associated with pathogenicity and bacterial fitness. Understanding of these large assemblies has exponentially increased in the last few years thanks to electron microscopy. In fact, a revolution in this field has led to breakthroughs in characterizing the structures of secretion systems and other macromolecular machineries so as to obtain high-resolution images of complexes that could not be crystallized. In this review, we give a brief overview of structural advancements in the understanding of secretion systems, focusing in particular on cryo–electron microscopy, whether tomography or single-particle analysis. We describe how such techniques have contributed to knowledge of the mechanism of macromolecule secretion in bacteria and the impact they will have in the future.

Bibliography

Rapisarda, C., Tassinari, M., Gubellini, F., & Fronzes, R. (2018). Using Cryo-EM to Investigate Bacterial Secretion Systems. Annual Review of Microbiology, 72(1), 231â254.

Authors 4

Chiara Rapisarda (first)
Matteo Tassinari (additional)
Francesca Gubellini (additional)
Rémi Fronzes (additional)

References 120 Referenced 17

10.1038/srep23080
10.4049/jimmunol.1101457
10.1128/MMBR.00023-09
10.1016/j.plasmid.2013.03.010
5. Ates LS, Houben ENG, Bitter W. 2016. Type VII secretion: a highly versatile secretion system. In Virulence Mechanisms of Bacterial Pathogens, ed. IT Kudva, NA Cornick, PJ Plummer, Q Zhang, TL Nicholson, et al., pp. 357–84. Washington, DC: Am. Soc. Microb. 5th ed. (10.1128/9781555819286.ch13)
10.1371/journal.ppat.1005696
10.2217/fmb.15.32
10.1046/j.1365-2958.2002.02816.x
10.1038/nature10846
10.1073/pnas.0609535104
10.1038/nmicrobiol.2017.47
10.1126/science.284.5419.1520
10.1126/science.aan7904
10.1002/embr.201337936
10.1371/journal.pgen.1005545
10.1128/JB.186.14.4645-4654.2004
10.1128/JB.00114-13
10.1098/rstb.2011.0209
10.1126/science.1095211
10.1074/jbc.M504463200
10.1038/nature08588
10.15252/embr.201744072
10.1126/science.aad2001
10.1016/j.celrep.2018.03.085
10.1128/ecosalplus.ESP-0020-2015
10.1016/j.cell.2015.02.005
10.1128/JB.183.13.3825-3832.2001
10.1016/j.cell.2016.08.025
10.1002/j.1460-2075.1987.tb02679.x
10.1098/rstb.2011.0204
10.1111/j.1365-2818.1981.tb02483.x
10.1371/journal.ppat.1003117
10.1038/nature14667
10.1074/jbc.M111.338731
10.1016/j.str.2015.10.023
{'issue': '1', 'key': 'B36', 'first-page': '305', 'volume': '4', 'author': 'Fan E', 'year': '2016', 'journal-title': 'Microbiol. Spectr.'} / Microbiol. Spectr. by Fan E (2016)
10.1078/1438-4221-00199
10.1016/S0304-3991(75)80020-9
10.1128/mBio.02001-15
10.1126/science.1166101
10.1038/nrmicro2218
10.1126/science.1166101
10.1146/annurev-micro-092412-155725
10.1128/MMBR.67.1.16-37.2003
10.15252/embr.201643598
10.1038/nature13768
{'key': 'B47', 'first-page': 'e00521', 'volume': '200', 'author': 'Hay ID', 'year': '2018', 'journal-title': 'Bacteriol'} / Bacteriol by Hay ID (2018)
10.1128/mBio.01344-17
10.1017/S003358350000305X
10.1016/S0022-2836(05)80271-2
10.1111/j.1365-2958.1993.tb01949.x
10.1016/j.cell.2017.02.022
10.1073/pnas.1411610112
10.1128/MMBR.62.2.379-433.1998 / Microbiol. Mol. Biol. Rev. by Hueck CJ (1998)
10.1016/j.cell.2017.04.010
10.1126/science.1091422
10.1111/j.1574-6968.2011.02464.x
10.1046/j.1365-2958.1997.6141981.x
10.1016/j.celrep.2014.05.034
10.1073/pnas.1404506111
10.7554/eLife.00792
10.1016/j.cell.2015.01.037
10.1126/science.1251652
64. Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J, et al. 2018. Structure of the core of the type three secretion system export apparatus. bioRxiv 249128. https://doi.org/10.1101/249128 (10.1101/249128)
10.3389/fcimb.2017.00215
10.1016/S0378-1097(03)00430-0
10.1038/nmeth.2472
10.1111/j.1365-2958.1996.tb02499.x
{'key': 'B69', 'first-page': '1635', 'volume': '16351997', 'author': 'Linderoth NA', 'year': '2008', 'journal-title': 'Science'} / Science by Linderoth NA (2008)
10.1038/s41564-017-0041-2
10.1111/mmi.13575
10.1038/nature13081
10.1016/j.sbi.2018.02.008
10.1038/srep33341
10.1038/nature04822
10.1126/science.1102610
10.1016/j.str.2017.01.010
10.1038/ncomms10114
10.15252/embj.201797103
10.1016/j.tim.2007.06.006
10.1016/j.str.2014.03.001
10.1016/j.bbamcr.2013.12.020
10.1128/microbiolspec.VMBF-0004-2015 / Microbiol. Spectr. by Notti RQ (2016)
10.1073/pnas.96.14.8173
10.1016/S0962-8924(99)01634-7
10.1099/mic.0.000197
10.1111/mmi.12744
10.15252/embj.201694024
10.1128/mr.57.1.50-108.1993 / Microbiol. Rev. by Pugsley AP (1993)
10.1111/j.1365-2958.1991.tb02115.x
{'issue': '3', 'key': 'B90', 'first-page': '709', 'volume': '46', 'author': 'Pym AS', 'year': '2002', 'journal-title': 'Microbiol'} / Microbiol by Pym AS (2002)
10.1038/nsmb.2722
10.21775/9781910190692.01
10.15252/embj.201796629
10.1038/nsmb.1910
10.1038/emboj.2013.58
10.1016/j.cell.2015.03.040
10.1038/nature10244
10.1016/j.str.2017.12.005
10.1002/j.1460-2075.1995.tb07155.x
10.1016/j.jsb.2012.09.006
10.1371/journal.ppat.1000824
10.1126/science.1199358
10.1038/nature12453
10.1038/nsmb.1603
10.1016/j.jsb.2006.05.009
10.1016/j.str.2014.07.005
10.1128/JB.00615-17
10.1016/j.tim.2016.11.004
10.1093/emboj/20.23.6735
10.1016/bs.mie.2016.04.014
10.1038/s41564-017-0020-7
10.1146/annurev.cellbio.21.012704.131001
10.1099/0022-1317-50-2-116
{'key': 'B115', 'first-page': '627', 'volume-title': 'Tuberculosis and the Tubercle Bacillus', 'author': 'Wong K-W', 'year': '2018'} / Tuberculosis and the Tubercle Bacillus by Wong K-W (2018)
10.1038/nature20576
10.1038/nsmb.3350
10.1038/nature03554
10.1096/fj.15-270843
10.1038/nature17182

Dates

Type	When
Created	7 years, 1 month ago (July 13, 2018, 3:24 p.m.)
Deposited	3 years, 10 months ago (Oct. 14, 2021, 8:55 a.m.)
Indexed	1 week, 1 day ago (Aug. 20, 2025, 8:54 a.m.)
Issued	6 years, 11 months ago (Sept. 8, 2018)
Published	6 years, 11 months ago (Sept. 8, 2018)
Published Print	6 years, 11 months ago (Sept. 8, 2018)

Funders 0

None

BibTeX

@article{Rapisarda_2018, title={Using Cryo-EM to Investigate Bacterial Secretion Systems}, volume={72}, ISSN={1545-3251}, url={http://dx.doi.org/10.1146/annurev-micro-090817-062702}, DOI={10.1146/annurev-micro-090817-062702}, number={1}, journal={Annual Review of Microbiology}, publisher={Annual Reviews}, author={Rapisarda, Chiara and Tassinari, Matteo and Gubellini, Francesca and Fronzes, Rémi}, year={2018}, month=sep, pages={231–254} }

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