Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types

Background and purpose: Our previous studies showed that lugdunin activities are associated with Staphylococcus lugdunensis genotypes, and most isolates do not exhibit lugdunin activity. As a continuation of our previous analysis, we focused on the reasons for defects in lugdunin production in S. lu...

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Main Authors: Lee-Chung Lin, Cheng-Yen Kao, Shih-Cheng Chang, Jazon Harl Hidrosollo, Jang-Jih Lu
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:Journal of Microbiology, Immunology and Infection
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1684118224000069
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author Lee-Chung Lin
Cheng-Yen Kao
Shih-Cheng Chang
Jazon Harl Hidrosollo
Jang-Jih Lu
author_facet Lee-Chung Lin
Cheng-Yen Kao
Shih-Cheng Chang
Jazon Harl Hidrosollo
Jang-Jih Lu
author_sort Lee-Chung Lin
collection DOAJ
description Background and purpose: Our previous studies showed that lugdunin activities are associated with Staphylococcus lugdunensis genotypes, and most isolates do not exhibit lugdunin activity. As a continuation of our previous analysis, we focused on the reasons for defects in lugdunin production in S. lugdunensis clinical isolates. Methods: A comparative analysis of 36 S. lugdunensis whole genome sequencing data revealed three major mutation types, unknown deletion mechanism that caused most of lug operon genes lost, mobile genetic element (MGE) insertion, and nonsense mutations, which potentially damaged lugdunin production. A total of 152 S. lugdunensis clinical isolates belonging to lugdunin nonproducers were further examined for the above three mutation types. PCR products were sequenced to examine these variations. Results: Forty-six of the 152 isolates were CRISPR-Cas IIC isolates, including 26 ST27, 14 ST4, and 6 ST29 isolates; further investigation confirmed that all of their lug operons had lost almost all lug operon genes except lugM. An IS256 insertion in lugA was identified in 16 isolates, and most isolates (15 over 16) belonged to ST3. In addition, three nonsense mutations caused by single nucleotide substitutions (an adenine deletion in lugB at the 361th and 1219th nucleotides and an adenine deletion in lugC at the 1612nd nucleotide) that were frequently observed among 36 S. lugdunensis whole genome sequencing data were further observed in our clinical isolates. These three nonsense mutations were frequently found in most of CRISPR-Cas IIIA strains, especially in ST6 isolates. Conclusion: Our findings suggest that the mechanisms affecting lugdunin production are associated with S. lugdunensis molecular types.
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spelling doaj.art-8a4549305fbe4ff6a7530a6cc2e8266b2024-03-23T06:23:30ZengElsevierJournal of Microbiology, Immunology and Infection1684-11822024-04-01572278287Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic typesLee-Chung Lin0Cheng-Yen Kao1Shih-Cheng Chang2Jazon Harl Hidrosollo3Jang-Jih Lu4Department of Laboratory Medicine, Linkou Chang Gung Memorial Hospital, Taoyuan, TaiwanInstitute of Microbiology and Immunology, College of Life Sciences, National Yang Ming Chiao Tung University, Taipei, TaiwanDepartment of Medical Laboratory, Linkou Chang Gung Memorial Hospital, Taoyuan, Taiwan; Department of Medical Biotechnology and Laboratory Science, College of Medicine, Chang Gung University, Taoyuan, TaiwanInstitute of Microbiology and Immunology, College of Life Sciences, National Yang Ming Chiao Tung University, Taipei, Taiwan; University of San Agustin, College of Pharmacy and Medical Technology, Iloilo City, PhilippinesDepartment of Laboratory Medicine, Linkou Chang Gung Memorial Hospital, Taoyuan, Taiwan; Department of Medical Biotechnology and Laboratory Science, College of Medicine, Chang Gung University, Taoyuan, Taiwan; Department of Medicine, College of Medicine, Chang Gung University, Taoyuan, Taiwan; Corresponding author. Department of Laboratory Medicine, Chang Gung Memorial Hospital, Lin-Kou, 5 Fu-Shing St. Kweishan, Taoyuan 333, Taiwan.Background and purpose: Our previous studies showed that lugdunin activities are associated with Staphylococcus lugdunensis genotypes, and most isolates do not exhibit lugdunin activity. As a continuation of our previous analysis, we focused on the reasons for defects in lugdunin production in S. lugdunensis clinical isolates. Methods: A comparative analysis of 36 S. lugdunensis whole genome sequencing data revealed three major mutation types, unknown deletion mechanism that caused most of lug operon genes lost, mobile genetic element (MGE) insertion, and nonsense mutations, which potentially damaged lugdunin production. A total of 152 S. lugdunensis clinical isolates belonging to lugdunin nonproducers were further examined for the above three mutation types. PCR products were sequenced to examine these variations. Results: Forty-six of the 152 isolates were CRISPR-Cas IIC isolates, including 26 ST27, 14 ST4, and 6 ST29 isolates; further investigation confirmed that all of their lug operons had lost almost all lug operon genes except lugM. An IS256 insertion in lugA was identified in 16 isolates, and most isolates (15 over 16) belonged to ST3. In addition, three nonsense mutations caused by single nucleotide substitutions (an adenine deletion in lugB at the 361th and 1219th nucleotides and an adenine deletion in lugC at the 1612nd nucleotide) that were frequently observed among 36 S. lugdunensis whole genome sequencing data were further observed in our clinical isolates. These three nonsense mutations were frequently found in most of CRISPR-Cas IIIA strains, especially in ST6 isolates. Conclusion: Our findings suggest that the mechanisms affecting lugdunin production are associated with S. lugdunensis molecular types.http://www.sciencedirect.com/science/article/pii/S1684118224000069Staphylococcus lugdunensisLugduninSequencing typesCRISPR-Cas IICUnknown deletion mechanismIS256
spellingShingle Lee-Chung Lin
Cheng-Yen Kao
Shih-Cheng Chang
Jazon Harl Hidrosollo
Jang-Jih Lu
Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types
Journal of Microbiology, Immunology and Infection
Staphylococcus lugdunensis
Lugdunin
Sequencing types
CRISPR-Cas IIC
Unknown deletion mechanism
IS256
title Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types
title_full Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types
title_fullStr Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types
title_full_unstemmed Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types
title_short Molecular characterization of lugdunin inactivation mechanisms and their association with Staphylococcus lugdunensis genetic types
title_sort molecular characterization of lugdunin inactivation mechanisms and their association with staphylococcus lugdunensis genetic types
topic Staphylococcus lugdunensis
Lugdunin
Sequencing types
CRISPR-Cas IIC
Unknown deletion mechanism
IS256
url http://www.sciencedirect.com/science/article/pii/S1684118224000069
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