Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome

被引:34
作者
Wang, Yueying [1 ]
Liu, Fang [2 ]
Urban, Joseph F., Jr. [3 ]
Paerewijck, Oonagh [4 ]
Geldhof, Peter [4 ]
Li, Robert W. [5 ]
机构
[1] Henan Agr Univ, Coll Anim Husb & Vet Sci, Minist Agr, Key Lab Anim Biochem & Nutr, Zhengzhou, Henan, Peoples R China
[2] Ocean Univ China, Coll Food Sci & Engn, Qingdao, Shandong, Peoples R China
[3] ARS, USDA, Beltsville Human Nutr Res Ctr, Diet Genom & Immunol Lab, Beltsville, MD USA
[4] Univ Ghent, Fac Vet Med, Lab Parasitol, Dept Virol Parasitol & Immunol, Merelbeke, Belgium
[5] ARS, USDA, Anim Parasit Dis Lab, Beltsville, MD 20705 USA
关键词
16S rRNA gene; Ascaris suum; Infection; Microbiome; Network; Swine; HELMINTH-PARASITES; GLUCOSE-TOLERANCE; TRICHURIS-SUIS; PIGS; INTESTINE; PATTERNS; BACTERIA; IMMUNITY; COLITIS; IMPACT;
D O I
10.1016/j.ijpara.2018.10.007
中图分类号
R38 [医学寄生虫学]; Q [生物科学];
学科分类号
07 ; 0710 ; 09 ; 100103 ;
摘要
The effect of infection of pigs with Ascaris suum on the microbial composition in the proximal colon and fecal matter was investigated using 16S rRNA gene sequencing. The infection significantly decreased various microbial diversity indices including Chao1 richness, but the effect on Chao1 in the colon luminal contents was worm burden-independent. The abundance of 49 genera present in colon contents, such as Prevotella and Faecalibacterium, and 179 operational taxonomic units was significantly changed as a result of infection. Notably, infection was also associated with a significant shift in the metabolic potential of the proximal colon microbiome, where the relative abundance of at least 30 metabolic pathways including carbohydrate metabolism and amino acid metabolism was reduced, while the abundance of 28 pathways was increased by infection. Furthermore, the microbial co-occurrence network in infected pigs was highly modular. Two of 52 modules or subnetworks were negatively correlated with fecal butyrate concentrations (r < -0.7; P < 0.05) while one module with 18 members was negatively correlated with fecal acetate, propionate and total short-chain fatty acids. A partial Mantel test identified a strong positive correlation between node connectivity of the operational taxonomic units assigned to beta-Proteobacteria (especially the family Alcaligenaceae) and fecal acetate and propionate levels (r = 0.82 and 0.74, respectively), while that of the family Porphyromonadaceae was positively correlated with fecal egg counts. Overall, Ascaris infection was associated with a profound change in the gut microbiome, especially in the proximity of the initial site of larval infection, and should facilitate our understanding of the pathophysiological consequence of gastrointestinal nematode infections. (C) 2019 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved.
引用
收藏
页码:247 / 256
页数:10
相关论文
共 58 条
[1]   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)
[2]   Verrucomicrobia Are Candidates for Polysaccharide-Degrading Bacterioplankton in an Arctic Fjord of Svalbard [J].
Cardman, Z. ;
Arnosti, C. ;
Durbin, A. ;
Ziervogel, K. ;
Cox, C. ;
Steen, A. D. ;
Teske, A. .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2014, 80 (12) :3749-3756
[3]   Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum [J].
Dawson, HD ;
Beshah, E ;
Nishi, S ;
Solano-Aguilar, G ;
Morimoto, M ;
Zhao, AP ;
Madden, KB ;
Ledbetter, TK ;
Dubey, JP ;
Shea-Donohue, T ;
Lunney, JK ;
Urban, JF .
INFECTION AND IMMUNITY, 2005, 73 (02) :1116-1128
[4]   Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa [J].
De Filippo, Carlotta ;
Cavalieri, Duccio ;
Di Paola, Monica ;
Ramazzotti, Matteo ;
Poullet, Jean Baptiste ;
Massart, Sebastien ;
Collini, Silvia ;
Pieraccini, Giuseppe ;
Lionetti, Paolo .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (33) :14691-14696
[5]   Molecular ecological network analyses [J].
Deng, Ye ;
Jiang, Yi-Huei ;
Yang, Yunfeng ;
He, Zhili ;
Luo, Feng ;
Zhou, Jizhong .
BMC BIOINFORMATICS, 2012, 13
[6]   Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis [J].
Flint, Harry J. ;
Bayer, Edward A. ;
Rincon, Marco T. ;
Lamed, Raphael ;
White, Bryan A. .
NATURE REVIEWS MICROBIOLOGY, 2008, 6 (02) :121-131
[7]   Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects [J].
Giacomin, Paul ;
Zakrzewski, Martha ;
Croese, John ;
Su, Xiaopei ;
Sotillo, Javier ;
McCann, Leisa ;
Navarro, Severine ;
Mitreva, Makedonka ;
Krause, Lutz ;
Loukas, Alex ;
Cantacessi, Cinzia .
SCIENTIFIC REPORTS, 2015, 5
[8]  
Harris D.L., 1971, Iowa State University Veterinarian, V33, P4
[9]   Interactions Between the Microbiota and the Immune System [J].
Hooper, Lora V. ;
Littman, Dan R. ;
Macpherson, Andrew J. .
SCIENCE, 2012, 336 (6086) :1268-1273
[10]   Effects of indigestible carbohydrates in barley on glucose metabolism, appetite and voluntary food intake over 16 h in healthy adults [J].
Johansson, Elin V. ;
Nilsson, Anne C. ;
Ostman, Elin M. ;
Bjorck, Inger M. E. .
NUTRITION JOURNAL, 2013, 12