Contribution of Extracellular Membrane Vesicles To the Secretome of Staphylococcus aureus

被引:10
作者
Uppu, Divakara S. S. M. [1 ,2 ]
Wang, Xiaogang [1 ,2 ]
Lee, Jean C. C. [1 ,2 ]
机构
[1] Brigham & Womens Hosp, Dept Med, Div Infect Dis, Boston, MA 02115 USA
[2] Harvard Med Sch, Boston, MA 02115 USA
来源
MBIO | 2023年 / 14卷 / 01期
关键词
Staphylococcus aureus; extracellular membrane vesicle; secretome; proteomics; membrane proteins; CAPSULAR POLYSACCHARIDE; EXCRETION; PATHOGENESIS; VIRULENCE; PEPTIDES; PROTEINS; ACID;
D O I
10.1128/mbio.03571-22
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
The secretome of Staphylococcus aureus includes soluble molecules and nano-sized extracellular membrane vesicles (MVs). The protein composition of both the secretome and MVs includes cytoplasmic and membrane proteins, as well as exoproteins, some cell wall-associated proteins, and glycopolymers. The microbial secretome modulates how the organism interacts with its environment. Included in the Staphylococcus aureus secretome are extracellular membrane vesicles (MVs) that consist of cytoplasmic and membrane proteins, as well as exoproteins, some cell wall-associated proteins, and glycopolymers. The extent to which MVs contribute to the diverse composition of the secretome is not understood. We performed a proteomic analysis of MVs purified from the S. aureus strain MRSA252 along with a similar analysis of the whole secretome (culture supernatant) before and after depletion of MVs. The MRSA252 secretome was comprised of 1,001 proteins, of which 667 were also present in MVs. Cell membrane-associated proteins and lipoteichoic acid in the culture supernatant were highly associated with MVs, followed by cytoplasmic and extracellular proteins. Few cell wall-associated proteins were contained in MVs, and capsular polysaccharides were found both in the secretome and MVs. When MVs were removed from the culture supernatant by ultracentrifugation, 54 of the secretome proteins were significantly depleted in abundance. Proteins packaged in MVs were characterized by an isoelectric point that was significantly higher than that of proteins excluded from MVs. Our data indicate that the generation of S. aureus MVs is a mechanism by which lipoteichoic acid, cytoplasmic, and cell membrane-associated proteins are released into the secretome.IMPORTANCE The secretome of Staphylococcus aureus includes soluble molecules and nano-sized extracellular membrane vesicles (MVs). The protein composition of both the secretome and MVs includes cytoplasmic and membrane proteins, as well as exoproteins, some cell wall-associated proteins, and glycopolymers. How the MV cargo differs from the protein composition of the secretome has not yet been addressed. Although the compositions of the secretome and MVs were strikingly similar, we identified 54 proteins that were specifically packaged in MVs. Proteins highly associated with MVs were characterized by their abundance in the secretome, an association with the bacterial membrane, and a basic isoelectric point. This study deepens our limited understanding about the contribution of MVs to the secretome of S. aureus.
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页数:13
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共 54 条
[1]   Antibiotics Stimulate Formation of Vesicles in Staphylococcus aureus in both Phage-Dependent and - Independent Fashions and via Different Routes [J].
Andreoni, Federica ;
Toyofuku, Masanori ;
Menzi, Carmen ;
Kalawong, Ratchara ;
Shambat, Srikanth Mairpady ;
Francois, Patrice ;
Zinkernagel, Annelies S. ;
Eberl, Leo .
ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, 2019, 63 (02)
[2]   Staphylococcus aureus Membrane-Derived Vesicles Promote Bacterial Virulence and Confer Protective Immunity in Murine Infection Models [J].
Askarian, Fatemeh ;
Lapek, John D., Jr. ;
Dongre, Mitesh ;
Tsai, Chih-Ming ;
Kumaraswamy, Monika ;
Kousha, Armin ;
Valderrama, J. Andres ;
Ludviksen, Judith A. ;
Cavanagh, Jorunn P. ;
Uchiyama, Satoshi ;
Mollnes, Tom E. ;
Gonzalez, David J. ;
Wai, Sun N. ;
Nizet, Victor ;
Johannessen, Mona .
FRONTIERS IN MICROBIOLOGY, 2018, 9
[3]   Release of protein A from the cell wall of Staphylococcus aureus [J].
Becker, Samuel ;
Frankel, Matthew B. ;
Schneewind, Olaf ;
Missiakas, Dominique .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (04) :1574-1579
[4]   Role of the Twin-Arginine Translocation Pathway in Staphylococcus [J].
Biswas, Lalitha ;
Biswas, Raja ;
Nerz, Christiane ;
Ohlsen, Knut ;
Schlag, Martin ;
Schaefer, Tina ;
Lamkemeyer, Tobias ;
Ziebandt, Anne-Kathrin ;
Hantke, Klaus ;
Rosenstein, Ralf ;
Goetz, Friedrich .
JOURNAL OF BACTERIOLOGY, 2009, 191 (19) :5921-5929
[5]   Staphylococcus aureus membrane vesicles contain immunostimulatory DNA, RNA and peptidoglycan that activate innate immune receptors and induce autophagy [J].
Bitto, Natalie J. ;
Cheng, Lesley ;
Johnston, Ella L. ;
Pathirana, Rishi ;
Phan, Thanh Kha ;
Poon, Ivan K. H. ;
O'Brien-Simpson, Neil M. ;
Hill, Andrew F. ;
Stinear, Timothy P. ;
Kaparakis-Liaskos, Maria .
JOURNAL OF EXTRACELLULAR VESICLES, 2021, 10 (06)
[6]   The Type VII Secretion System of Staphylococcus [J].
Bowman, Lisa ;
Palmer, Tracy .
ANNUAL REVIEW OF MICROBIOLOGY, VOL 75, 2021, 2021, 75 :471-494
[7]   Temperature Influences the Composition and Cytotoxicity of Extracellular Vesicles in Staphylococcus aureus [J].
Briaud, Paul ;
Frey, Andrew ;
Marino, Emily C. ;
Bastock, Raeven A. ;
Zielinski, Riley E. ;
Wiemels, Richard E. ;
Keogh, Rebecca A. ;
Murphy, Erin R. ;
Shaw, Lindsey N. ;
Carroll, Ronan K. .
MSPHERE, 2021, 6 (05)
[8]   Extracellular vesicles produced by the Gram-positive bacterium Bacillus subtilis are disrupted by the lipopeptide surfactin [J].
Brown, Lisa ;
Kessler, Anne ;
Cabezas-Sanchez, Pablo ;
Luque-Garcia, Jose L. ;
Casadevall, Arturo .
MOLECULAR MICROBIOLOGY, 2014, 93 (01) :183-198
[9]   EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections [J].
Burts, ML ;
Williams, WA ;
DeBord, K ;
Missiakas, DM .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (04) :1169-1174
[10]   The Capsular Polysaccharide of Staphylococcus aureus Is Attached to Peptidoglycan by the LytR-CpsA-Psr (LCP) Family of Enzymes [J].
Chan, Yvonne Gar-Yun ;
Kim, Hwan Keun ;
Schneewind, Olaf ;
Missiakas, Dominique .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2014, 289 (22) :15680-15690