The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus

ABSTRACT Emerging studies reveal unique bacterial communities in the human bladder, with alteration of composition associated to disease states. Systemic lupus erythematosus (SLE) is a complex autoimmune disease that is characterized by frequent impairment of the kidney. Here, we explored the bladde...

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Main Authors: Fengping Liu, Jingjie Du, Qixiao Zhai, Jialin Hu, Aaron W. Miller, Tianli Ren, Yangkun Feng, Peng Jiang, Lei Hu, Jiayi Sheng, Chaoqun Gu, Ren Yan, Longxian Lv, Alan J. Wolfe, Ninghan Feng
Format: Article
Language:English
Published: American Society for Microbiology 2022-10-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.00212-22
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author Fengping Liu
Jingjie Du
Qixiao Zhai
Jialin Hu
Aaron W. Miller
Tianli Ren
Yangkun Feng
Peng Jiang
Lei Hu
Jiayi Sheng
Chaoqun Gu
Ren Yan
Longxian Lv
Alan J. Wolfe
Ninghan Feng
author_facet Fengping Liu
Jingjie Du
Qixiao Zhai
Jialin Hu
Aaron W. Miller
Tianli Ren
Yangkun Feng
Peng Jiang
Lei Hu
Jiayi Sheng
Chaoqun Gu
Ren Yan
Longxian Lv
Alan J. Wolfe
Ninghan Feng
author_sort Fengping Liu
collection DOAJ
description ABSTRACT Emerging studies reveal unique bacterial communities in the human bladder, with alteration of composition associated to disease states. Systemic lupus erythematosus (SLE) is a complex autoimmune disease that is characterized by frequent impairment of the kidney. Here, we explored the bladder microbiome, metabolome, and cytokine profiles in SLE patients, as well as correlations between microbiome and metabolome, cytokines, and disease profiles. We recruited a group of 50 SLE patients and 50 individually matched asymptomatic controls. We used transurethral catheterization to collect urine samples, 16S rRNA gene sequencing to profile bladder microbiomes, and liquid chromatography-tandem mass spectrometry to perform untargeted metabolomic profiling. Compared to controls, SLE patients possessed unique bladder microbial communities and increased alpha diversity. These differences were accompanied by differences in urinary metabolomes, cytokines, and patients’ disease profiles. The SLE-enriched genera, including Bacteroides, were positively correlated with several SLE-enriched metabolites, including olopatadine. The SLE-depleted genera, such as Pseudomonas, were negatively correlated to SLE-depleted cytokines, including interleukin-8. Alteration of the bladder microbiome was associated with disease profile. For example, the genera Megamonas and Phocaeicola were negatively correlated with serum complement component 3, and Streptococcus was positively correlated with IgG. Our present study reveals associations between the bladder microbiome and the urinary metabolome, cytokines, and disease phenotypes. Our results could help identify biomarkers for SLE. IMPORTANCE Contrary to dogma, the human urinary bladder possesses its own unique bacterial community with alteration of composition associated with disease states. Systemic lupus erythematosus (SLE) is a complex autoimmune disease often characterized by kidney impairment. Here, we explored the bladder microbiome, metabolome, and cytokine profiles in SLE patients, as well as correlations between the microbiome and metabolome, cytokines, and disease profiles. Compared to controls, SLE patients possessed a unique bladder microbial community and elevated alpha diversity. These differences were accompanied by differences in bladder metabolomes, cytokines, and patients’ disease profiles. SLE-enriched genera were positively correlated with several SLE-enriched metabolites. SLE-depleted genera were negatively correlated to SLE-depleted cytokines. Alteration of the bladder microbiome was associated with disease profile. Thus, our study reveals associations between the bladder microbiome and the bladder metabolome, cytokines, and disease phenotypes. These results could help identify biomarkers for SLE.
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spelling doaj.art-62482e20c2f84d2ebbc8981ad218bd202022-12-22T04:33:13ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.00212-22The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus ErythematosusFengping Liu0Jingjie Du1Qixiao Zhai2Jialin Hu3Aaron W. Miller4Tianli Ren5Yangkun Feng6Peng Jiang7Lei Hu8Jiayi Sheng9Chaoqun Gu10Ren Yan11Longxian Lv12Alan J. Wolfe13Ninghan Feng14Wuxi School of Medicine, Jiangnan University, Wuxi, Jiangsu, ChinaDepartment of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USAState Key Laboratory of Food Science and Technology and School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, ChinaDepartment of Urology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, Jiangsu, ChinaGlickman Urological and Kidney Institute, Cleveland, Ohio, USADepartment of Rheumatology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, ChinaSchool of Medicine, Nantong University, Nantong, Jiangsu, ChinaDepartment of Urology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, Jiangsu, ChinaDepartment of Urology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, Jiangsu, ChinaDepartment of Urology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, Jiangsu, ChinaDepartment of Urology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, Jiangsu, ChinaCollaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, ChinaSchool of Medicine, Nantong University, Nantong, Jiangsu, ChinaDepartment of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USADepartment of Urology, Affiliated Wuxi No. 2 Hospital, Nanjing Medical University, Wuxi, Jiangsu, ChinaABSTRACT Emerging studies reveal unique bacterial communities in the human bladder, with alteration of composition associated to disease states. Systemic lupus erythematosus (SLE) is a complex autoimmune disease that is characterized by frequent impairment of the kidney. Here, we explored the bladder microbiome, metabolome, and cytokine profiles in SLE patients, as well as correlations between microbiome and metabolome, cytokines, and disease profiles. We recruited a group of 50 SLE patients and 50 individually matched asymptomatic controls. We used transurethral catheterization to collect urine samples, 16S rRNA gene sequencing to profile bladder microbiomes, and liquid chromatography-tandem mass spectrometry to perform untargeted metabolomic profiling. Compared to controls, SLE patients possessed unique bladder microbial communities and increased alpha diversity. These differences were accompanied by differences in urinary metabolomes, cytokines, and patients’ disease profiles. The SLE-enriched genera, including Bacteroides, were positively correlated with several SLE-enriched metabolites, including olopatadine. The SLE-depleted genera, such as Pseudomonas, were negatively correlated to SLE-depleted cytokines, including interleukin-8. Alteration of the bladder microbiome was associated with disease profile. For example, the genera Megamonas and Phocaeicola were negatively correlated with serum complement component 3, and Streptococcus was positively correlated with IgG. Our present study reveals associations between the bladder microbiome and the urinary metabolome, cytokines, and disease phenotypes. Our results could help identify biomarkers for SLE. IMPORTANCE Contrary to dogma, the human urinary bladder possesses its own unique bacterial community with alteration of composition associated with disease states. Systemic lupus erythematosus (SLE) is a complex autoimmune disease often characterized by kidney impairment. Here, we explored the bladder microbiome, metabolome, and cytokine profiles in SLE patients, as well as correlations between the microbiome and metabolome, cytokines, and disease profiles. Compared to controls, SLE patients possessed a unique bladder microbial community and elevated alpha diversity. These differences were accompanied by differences in bladder metabolomes, cytokines, and patients’ disease profiles. SLE-enriched genera were positively correlated with several SLE-enriched metabolites. SLE-depleted genera were negatively correlated to SLE-depleted cytokines. Alteration of the bladder microbiome was associated with disease profile. Thus, our study reveals associations between the bladder microbiome and the bladder metabolome, cytokines, and disease phenotypes. These results could help identify biomarkers for SLE.https://journals.asm.org/doi/10.1128/spectrum.00212-22bladder microbiomecomplementdisease profilesystemic lupus erythematosusurinary cytokinesurinary metabolome
spellingShingle Fengping Liu
Jingjie Du
Qixiao Zhai
Jialin Hu
Aaron W. Miller
Tianli Ren
Yangkun Feng
Peng Jiang
Lei Hu
Jiayi Sheng
Chaoqun Gu
Ren Yan
Longxian Lv
Alan J. Wolfe
Ninghan Feng
The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus
Microbiology Spectrum
bladder microbiome
complement
disease profile
systemic lupus erythematosus
urinary cytokines
urinary metabolome
title The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus
title_full The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus
title_fullStr The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus
title_full_unstemmed The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus
title_short The Bladder Microbiome, Metabolome, Cytokines, and Phenotypes in Patients with Systemic Lupus Erythematosus
title_sort bladder microbiome metabolome cytokines and phenotypes in patients with systemic lupus erythematosus
topic bladder microbiome
complement
disease profile
systemic lupus erythematosus
urinary cytokines
urinary metabolome
url https://journals.asm.org/doi/10.1128/spectrum.00212-22
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