Thermonucleases Contribute to Staphylococcus aureus Biofilm Formation in Implant-Associated Infections–A Redundant and Complementary Story
Biofilms formed by Staphylococcus aureus are one of the predominant causes of implant-associated infections (IAIs). Previous studies have found that S. aureus nucleases nuc1 and nuc2 modulate biofilm formation. In this study, we found low nuc1 / nuc2 expression and high biofilm-forming ability among...
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| Published in: | Frontiers in microbiology Vol. 12; p. 687888 |
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| Main Authors: | , , , , , , , , , |
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| Abstract | Biofilms formed by
Staphylococcus aureus
are one of the predominant causes of implant-associated infections (IAIs). Previous studies have found that
S. aureus
nucleases
nuc1
and
nuc2
modulate biofilm formation. In this study, we found low
nuc1
/
nuc2
expression and high biofilm-forming ability among IAI isolates. Furthermore, in a mouse model of exogenous IAIs, Δ
nuc1/2
exhibited higher bacterial load on the surface of the implant than that exhibited by the other groups (WT, Δ
nuc1
, and Δ
nuc2
). Survival analysis of the hematogenous IAI mouse model indicated that
nuc1
is a virulence factor related to mortality. We then detected the influence of
nuc1
and
nuc2
on biofilm formation and immune evasion
in vitro
. Observation of
in vitro
biofilm structures with scanning electron microscopy and evaluation of bacterial aggregation with flow cytometry revealed that both
nuc1
and
nuc2
are involved in biofilm structuring and bacterial aggregation. Unlike
nuc1
, which is reported to participate in immune evasion,
nuc2
cannot degrade neutrophil extracellular traps. Moreover, we found that
nuc1
/
nuc2
transcription is negatively correlated during
S. aureus
growth, and a possible complementary relationship has been proposed. In conclusion,
nuc1
/
nuc2
are complementary genes involved in biofilm formation in exogenous IAIs. However,
nuc2
contributes less to virulence and is not involved in immune evasion. |
|---|---|
| AbstractList | Biofilms formed by
Staphylococcus aureus
are one of the predominant causes of implant-associated infections (IAIs). Previous studies have found that
S. aureus
nucleases
nuc1
and
nuc2
modulate biofilm formation. In this study, we found low
nuc1
/
nuc2
expression and high biofilm-forming ability among IAI isolates. Furthermore, in a mouse model of exogenous IAIs, Δ
nuc1/2
exhibited higher bacterial load on the surface of the implant than that exhibited by the other groups (WT, Δ
nuc1
, and Δ
nuc2
). Survival analysis of the hematogenous IAI mouse model indicated that
nuc1
is a virulence factor related to mortality. We then detected the influence of
nuc1
and
nuc2
on biofilm formation and immune evasion
in vitro
. Observation of
in vitro
biofilm structures with scanning electron microscopy and evaluation of bacterial aggregation with flow cytometry revealed that both
nuc1
and
nuc2
are involved in biofilm structuring and bacterial aggregation. Unlike
nuc1
, which is reported to participate in immune evasion,
nuc2
cannot degrade neutrophil extracellular traps. Moreover, we found that
nuc1
/
nuc2
transcription is negatively correlated during
S. aureus
growth, and a possible complementary relationship has been proposed. In conclusion,
nuc1
/
nuc2
are complementary genes involved in biofilm formation in exogenous IAIs. However,
nuc2
contributes less to virulence and is not involved in immune evasion. Biofilms formed by Staphylococcus aureus are one of the predominant causes of implant-associated infections (IAIs). Previous studies have found that S. aureus nucleases nuc1 and nuc2 modulate biofilm formation. In this study, we found low nuc1/nuc2 expression and high biofilm-forming ability among IAI isolates. Furthermore, in a mouse model of exogenous IAIs, Δnuc1/2 exhibited higher bacterial load on the surface of the implant than that exhibited by the other groups (WT, Δnuc1, and Δnuc2). Survival analysis of the hematogenous IAI mouse model indicated that nuc1 is a virulence factor related to mortality. We then detected the influence of nuc1 and nuc2 on biofilm formation and immune evasion in vitro. Observation of in vitro biofilm structures with scanning electron microscopy and evaluation of bacterial aggregation with flow cytometry revealed that both nuc1 and nuc2 are involved in biofilm structuring and bacterial aggregation. Unlike nuc1, which is reported to participate in immune evasion, nuc2 cannot degrade neutrophil extracellular traps. Moreover, we found that nuc1/nuc2 transcription is negatively correlated during S. aureus growth, and a possible complementary relationship has been proposed. In conclusion, nuc1/nuc2 are complementary genes involved in biofilm formation in exogenous IAIs. However, nuc2 contributes less to virulence and is not involved in immune evasion. |
| Author | Zhang, Feiyang Hamushan, Musha Mao, Yanjie Jiang, Feng Du, Jiafei Shen, Hao Tang, Jin Wang, Qiaojie Han, Pei Yu, Jinlong |
| AuthorAffiliation | 1 Department of Orthopedics, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital , Shanghai , China 2 Department of Clinical Laboratory, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital , Shanghai , China 3 Department of Orthopedics, Jinjiang Municipal Hospital , Fujian , China |
| AuthorAffiliation_xml | – name: 1 Department of Orthopedics, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital , Shanghai , China – name: 3 Department of Orthopedics, Jinjiang Municipal Hospital , Fujian , China – name: 2 Department of Clinical Laboratory, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital , Shanghai , China |
| Author_xml | – sequence: 1 givenname: Jinlong surname: Yu fullname: Yu, Jinlong – sequence: 2 givenname: Feng surname: Jiang fullname: Jiang, Feng – sequence: 3 givenname: Feiyang surname: Zhang fullname: Zhang, Feiyang – sequence: 4 givenname: Musha surname: Hamushan fullname: Hamushan, Musha – sequence: 5 givenname: Jiafei surname: Du fullname: Du, Jiafei – sequence: 6 givenname: Yanjie surname: Mao fullname: Mao, Yanjie – sequence: 7 givenname: Qiaojie surname: Wang fullname: Wang, Qiaojie – sequence: 8 givenname: Pei surname: Han fullname: Han, Pei – sequence: 9 givenname: Jin surname: Tang fullname: Tang, Jin – sequence: 10 givenname: Hao surname: Shen fullname: Shen, Hao |
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| CitedBy_id | crossref_primary_10_3389_fimmu_2022_836278 crossref_primary_10_1159_000530385 crossref_primary_10_3389_fmicb_2022_825041 crossref_primary_10_1007_s12010_024_04938_y crossref_primary_10_1021_acscentsci_3c00499 crossref_primary_10_3389_fmicb_2022_818307 crossref_primary_10_3389_fcimb_2024_1400648 crossref_primary_10_3389_fcimb_2021_799845 crossref_primary_10_4081_hls_2023_11527 crossref_primary_10_1002_cmdc_202200711 crossref_primary_10_3389_fimmu_2024_1355764 crossref_primary_10_1080_21505594_2023_2228657 crossref_primary_10_3389_fmicb_2023_1224085 crossref_primary_10_3390_molecules26144378 crossref_primary_10_14202_vetworld_2022_558_564 crossref_primary_10_3389_fimmu_2022_899890 |
| Cites_doi | 10.1016/j.copbio.2014.12.002 10.1093/bioinformatics/btm201 10.1016/j.arth.2013.07.021 10.1073/pnas.1703427114 10.1016/j.plasmid.2005.05.005 10.1111/joim.12233 10.1016/j.amjmed.2015.09.006 10.1007/s11427-011-4195-5 10.1128/microbiolspec.GPP3-0023-2018 10.1016/j.jinf.2011.05.005 10.1371/journal.pone.0095574 10.1128/IAI.00605-19 10.3390/microorganisms4040041 10.1016/j.cmi.2019.08.006 10.1016/S0140-6736(14)61798-0 10.1111/j.1574-695X.2012.00968.x 10.1007/s11999-008-0209-4 10.1128/IAI.01242-12 10.1093/femsre/fuv015 10.1159/000319909 10.1128/MMBR.00026-19 10.1089/fpd.2011.1033 10.1111/j.1574-6968.2008.01194.x 10.1126/science.295.5559.1487 10.1007/s11999-017-5266-0 10.1038/srep43889 10.1126/science.1242255 10.1111/j.1574-695X.2012.00938.x 10.1038/nrmicro2415 10.1177/039139880502801106 10.1038/s41579-018-0019-y 10.1007/7651_2014_186 10.1073/pnas.1805622115 10.1128/microbiolspec.VMBF-0022-2015 10.1155/2018/1067413 10.3389/fcimb.2015.00001 10.1128/IAI.06134-11 10.1126/science.1183021 10.1128/mBio.01341-14 10.1093/nar/gkv007 10.1371/journal.pone.0026714 10.1016/j.micpath.2011.04.007 10.1159/000319855 |
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| Copyright | Copyright © 2021 Yu, Jiang, Zhang, Hamushan, Du, Mao, Wang, Han, Tang and Shen. 2021 Yu, Jiang, Zhang, Hamushan, Du, Mao, Wang, Han, Tang and Shen |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Catherine Dunyach-Remy, INSERM U1047 Virulence Bactérienne et Maladies Infectieuses, France Reviewed by: Angela Maria Oliveira de Sousa França, University of Minho, Portugal; Anders P. Hakansson, Lund University, Sweden This article was submitted to Infectious Diseases, a section of the journal Frontiers in Microbiology |
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| Snippet | Biofilms formed by
Staphylococcus aureus
are one of the predominant causes of implant-associated infections (IAIs). Previous studies have found that
S. aureus... Biofilms formed by Staphylococcus aureus are one of the predominant causes of implant-associated infections (IAIs). Previous studies have found that S. aureus... |
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| StartPage | 687888 |
| SubjectTerms | biofilm implant associated infections Microbiology periprosthetic joint infection Staphylococcus aureus thermonuclease |
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| Title | Thermonucleases Contribute to Staphylococcus aureus Biofilm Formation in Implant-Associated Infections–A Redundant and Complementary Story |
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