Alterations of Gut Microbiome and Metabolite Profiling in Mice Infected bySchistosoma japonicum

被引:46
作者
Hu, Yue [1 ,2 ,3 ]
Chen, Jiansong [4 ]
Xu, Yiyue [1 ,2 ]
Zhou, Hongli [1 ,2 ]
Huang, Ping [1 ,2 ]
Ma, Yubin [1 ,2 ]
Gao, Minzhao [5 ]
Cheng, Shaoyun [1 ,2 ]
Zhou, Haiyun [4 ]
Lv, Zhiyue [1 ,2 ,3 ,6 ]
机构
[1] Sun Yat Sen Univ, Minist Educ, Key Lab Trop Dis Control, Guangzhou, Peoples R China
[2] Hainan Med Univ, Minist Educ, Key Lab Trop Translat Med, Haikou, Hainan, Peoples R China
[3] Sun Yat Sen Univ, Affiliated Hosp 5, Zhongshan Sch Med, Joint Program Pathobiol, Guangzhou, Peoples R China
[4] Sun Yat Sen Univ, Instrumental Anal & Res Ctr, Guangzhou, Peoples R China
[5] Sun Yat Sen Univ, Affiliated Hosp 5, Dept Gastroenterol, Zhuhai, Peoples R China
[6] Sun Yat Sen Univ, Zhongshan Sch Med, Prov Engn Technol Res Ctr Biol Vector Control, Guangzhou, Peoples R China
基金
中国国家自然科学基金;
关键词
Schistosoma japonicum; gut microbiome; metagenomics; metabolomics; 16SrRNA; UPLC-MS; 3; SCHISTOSOMA-JAPONICUM; FATTY-ACIDS; LYSOPHOSPHATIDYLCHOLINE; METABOLOMICS; SEQUENCES; PROTEIN; CHAIN;
D O I
10.3389/fimmu.2020.569727
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Schistosoma japonicum(S. japonicum) is one of the etiological agents of schistosomiasis, a widespread zoonotic parasitic disease. However, the mechanism of the balanced co-existence between the host immune system andS. japonicumas well as their complex interaction remains unclear. In this study,16SrRNA gene sequencing, combined with metagenomic sequencing approach as well as ultraperformance liquid chromatography-mass spectrometry metabolic profiling, was applied to demonstrate changes in the gut microbiome community structure during schistosomiasis progression, the functional interactions between the gut bacteria andS. japonicuminfection in BALB/c mice, and the dynamic metabolite changes of the host. The results showed that both gut microbiome and the metabolites were significantly altered at different time points after the infection. Decrease in richness and diversity as well as differed composition of the gut microbiota was observed in the infected status when compared with the uninfected status. At the phylum level, the gut microbial communities in all samples were dominated by Firmicutes, Bacteroidetes, Proteobacteria, and Deferribacteres, while at the genus level,Lactobacillus, Lachnospiraceae NK4A136 group, Bacteroides, Staphylococcus, andAlloprevotellawere the most abundant. After exposure,Roseburia, andRuminococcaceae UCG-014decreased, whileStaphylococcus, Alistipes, andParabacteroidesincreased, which could raise the risk of infections. Furthermore, LEfSe demonstrated several bacterial taxa that could discriminate between each time point ofS. japonicuminfection. Besides that, metagenomic analysis illuminated that the AMP-activated protein kinase (AMPK) signaling pathway and the chemokine signaling pathway were significantly perturbed after the infection. Phosphatidylcholine and colfosceril palmitate in serum as well as xanthurenic acid, naphthalenesulfonic acid, and pimelylcarnitine in urine might be metabolic biomarkers due to their promising diagnostic potential at the early stage of the infection. Alterations of glycerophospholipid and purine metabolism were also discovered in the infection. The present study might provide further understanding of the mechanisms during schistosome infection in aspects of gut microbiome and metabolites, and facilitate the discovery of new targets for early diagnosis and prognostic purposes. Further validations of potential biomarkers in human populations are necessary, and the exploration of interactions amongS. japonicum, gut microbiome, and metabolites is to be deepened in the future.
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页数:20
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共 83 条
[1]   Metabolite profiling for biomarkers in Schistosoma haematobium infection and associated bladder pathologies [J].
Adebayo, Adewale S. ;
Mundhe, Swapnil D. ;
Awobode, Henrietta O. ;
Onile, Olugbenga S. ;
Agunloye, Atinuke M. ;
Isokpehi, Raphael D. ;
Shouche, Yogesh S. ;
Santhakumari, Bayatigeri ;
Anumudu, Chiaka I. .
PLOS NEGLECTED TROPICAL DISEASES, 2018, 12 (04)
[2]   Trimmomatic: a flexible trimmer for Illumina sequence data [J].
Bolger, Anthony M. ;
Lohse, Marc ;
Usadel, Bjoern .
BIOINFORMATICS, 2014, 30 (15) :2114-2120
[3]   Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome [J].
Borton, Mikayla A. ;
Sabag-Daigle, Anice ;
Wu, Jikang ;
Solden, Lindsey M. ;
O'Banion, Bridget S. ;
Daly, Rebecca A. ;
Wolfe, Richard A. ;
Gonzalez, Juan F. ;
Wysocki, Vicki H. ;
Ahmer, Brian M. M. ;
Wrighton, Kelly C. .
MICROBIOME, 2017, 5
[4]   Wormholes in Host Defense: How Helminths Manipulate Host Tissues to Survive and Reproduce [J].
Boyett, Deborah ;
Hsieh, Michael H. .
PLOS PATHOGENS, 2014, 10 (04)
[5]   Therapeutic Helminth Infection of Macaques with Idiopathic Chronic Diarrhea Alters the Inflammatory Signature and Mucosal Microbiota of the Colon [J].
Broadhurst, Mara Jana ;
Ardeshir, Amir ;
Kanwar, Bittoo ;
Mirpuri, Julie ;
Gundra, Uma Mahesh ;
Leung, Jacqueline M. ;
Wiens, Kirsten E. ;
Vujkovic-Cvijin, Ivan ;
Kim, Charlie C. ;
Yarovinsky, Felix ;
Lerche, Nicholas W. ;
McCune, Joseph M. ;
Loke, P'ng .
PLOS PATHOGENS, 2012, 8 (11)
[6]   Polyunsaturated fatty acids, inflammation, and immunity [J].
Calder, PC .
LIPIDS, 2001, 36 (09) :1007-1024
[7]   QIIME allows analysis of high-throughput community sequencing data [J].
Caporaso, J. Gregory ;
Kuczynski, Justin ;
Stombaugh, Jesse ;
Bittinger, Kyle ;
Bushman, Frederic D. ;
Costello, Elizabeth K. ;
Fierer, Noah ;
Pena, Antonio Gonzalez ;
Goodrich, Julia K. ;
Gordon, Jeffrey I. ;
Huttley, Gavin A. ;
Kelley, Scott T. ;
Knights, Dan ;
Koenig, Jeremy E. ;
Ley, Ruth E. ;
Lozupone, Catherine A. ;
McDonald, Daniel ;
Muegge, Brian D. ;
Pirrung, Meg ;
Reeder, Jens ;
Sevinsky, Joel R. ;
Tumbaugh, Peter J. ;
Walters, William A. ;
Widmann, Jeremy ;
Yatsunenko, Tanya ;
Zaneveld, Jesse ;
Knight, Rob .
NATURE METHODS, 2010, 7 (05) :335-336
[8]   Profiling of the perturbed metabolomic state of mouse spleen during acute and chronic toxoplasmosis [J].
Chen, Xiao-Qing ;
Zhou, Chun-Xue ;
Elsheikha, Hany M. ;
He, Shuai ;
Hu, Gui-Xue ;
Zhu, Xing-Quan .
PARASITES & VECTORS, 2017, 10
[9]   Gut microbial-derived butyrate is inversely associated with IgE responses to allergens in childhood asthma [J].
Chiu, Chih-Yung ;
Cheng, Mei-Ling ;
Chiang, Meng-Han ;
Kuo, Yu-Lun ;
Tsai, Ming-Han ;
Chiu, Chun-Che ;
Lin, Gigin .
PEDIATRIC ALLERGY AND IMMUNOLOGY, 2019, 30 (07) :689-697
[10]   MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis [J].
Chong, Jasmine ;
Soufan, Othman ;
Li, Carin ;
Caraus, Iurie ;
Li, Shuzhao ;
Bourque, Guillaume ;
Wishart, David S. ;
Xia, Jianguo .
NUCLEIC ACIDS RESEARCH, 2018, 46 (W1) :W486-W494