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Gut Pathogens
Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

A human stool-derived Bilophila wadsworthia strain caused systemic inflammation in specific-pathogen-free mice

Authors: Zhou Feng, Wenmin Long, Binhan Hao, Ding Ding, Xiaoqing Ma, Liping Zhao, Xiaoyan Pang

Published in: Gut Pathogens | Issue 1/2017

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Abstract

Background

Bilophila wadsworthia is a major member of sulfidogenic bacteria in human gut, it was originally recovered from different clinical specimens of intra-abdominal infections and recently was reported potentially linked to different chronic metabolic disorders. However, there is still insufficient understanding on its detailed function and mechanism to date.

Methods

A B. wadsworthia strain was isolated from fresh feces of a latent autoimmune diabetes in adults patient and we investigated its pathogenicity by oral administration to specific-pathogen-free mice. Tissue samples and serum were collected after sacrifice. Stool samples were collected at different time points to profile the gut microbiota.

Results

Bilophila wadsworthia infection resulted in the reduction of body weight and fat mass, apparent hepatosplenomegaly and elevated serum inflammatory factors, including serum amyloid A and interleukin-6, while without significant change of the overall gut microbiota structure.

Conclusions

These results demonstrated that higher amount of B. wadsworthia caused systemic inflammatory response in SPF mice, which adds new evidence to the pathogenicity of this bacterium and implied its potential role to the chronic inflammation related metabolic diseases like diabetes.
Literature
1.
Fei N, Zhao L. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J. 2013;7(4):880–4.CrossRefPubMed
2.
Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA. 2013;110(22):9066–71.CrossRefPubMedPubMedCentral
3.
4.
Baron EJ, Summanen P, Downes J, Roberts MC, Wexler H, Finegold SM. Bilophila wadsworthia, gen. nov. and sp. nov., a unique gram-negative anaerobic rod recovered from appendicitis specimens and human faeces. J Gen Microbiol. 1989;135(12):3405–11.PubMed
5.
Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature. 2012;487(7405):104–8.PubMedPubMedCentral
6.
Yazici C, Wolf PG, Carroll TP, Mutlu E, Xicola RM, Llor X, et al. 511 Bilophila wadsworthia is more abundant in the colonic microbiome of colorectal cancer cases compared to healthy controls. Gastroenterology. 2015;148(4):100.CrossRef
7.
Liang T, Su W, Zhang Q, Li G, Gao S, Lou J, et al. Roles of sphincter of oddi laxity in bile duct microenvironment in patients with cholangiolithiasis: from the perspective of the microbiome and metabolome. J Am Coll Surg. 2016;222(3):269–80.CrossRefPubMed
8.
Sen T, Cawthon CR, Ihde BT, Hajnal A, Dilorenzo PM, De La Serre CB, et al. Diet-driven microbiota dysbiosis is associated with vagal remodeling and obesity. Physiol Behav. 2017;173:305–17.CrossRefPubMed
9.
Tremlett H, Fadrosh DW, Faruqi AA, Zhu F, Hart J, Roalstad S, et al. Gut microbiota in early pediatric multiple sclerosis: a case-control study. Eur J Neurol. 2016;23(8):1308–21.CrossRefPubMedPubMedCentral
10.
Zhang X, Zhao Y, Zhang M, Pang X, Xu J, Kang C, et al. Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS ONE. 2012;7(8):e42529.CrossRefPubMedPubMedCentral
11.
Laue H, Smits TH, Schumacher UK, Claros MC, Hartemink R, Cook AM. Identification of Bilophila wadsworthia by specific PCR which targets the taurine:pyruvate aminotransferase gene. FEMS Microbiol Lett. 2006;261(1):74–9.CrossRefPubMed
12.
Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology. 2002;148(Pt 1):257–66.CrossRefPubMed
13.
Loubinoux J, Bronowicki JP, Pereira IA, Mougenel JL, Faou AE. Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases. FEMS Microbiol Ecol. 2002;40(2):107–12.CrossRefPubMed
14.
Bayston R, Ashraf W, Barker-Davies R, Tucker E, Clement R, Clayton J, et al. Biofilm formation by Propionibacterium acnes on biomaterials in vitro and in vivo: impact on diagnosis and treatment. J Biomed Mater Res A. 2007;81(3):705–9.CrossRefPubMed
15.
Grant AJ, Foster GL, Mckinley TJ, Brown SP, Clare S, Maskell DJ, et al. Bacterial growth rate and host factors as determinants of intracellular bacterial distributions in systemic Salmonella enterica infections. Infect Immun. 2009;77(12):5608–11.CrossRefPubMedPubMedCentral
16.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8.CrossRefPubMed
17.
Zhang C, Yin A, Li H, Wang R, Wu G, Shen J, et al. Dietary modulation of gut microbiota contributes to alleviation of both genetic and simple obesity in children. EBioMedicine. 2015;2(8):968–84.CrossRefPubMedPubMedCentral
18.
Godon JJ, Zumstein E, Dabert P, Habouzit F, Moletta R. Molecular microbial diversity of an anaerobic digestor as determined by small-subunit rDNA sequence analysis. Appl Environ Microbiol. 1997;63(7):2802–13.PubMedPubMedCentral
19.
Zhang Q, Wu Y, Wang J, Wu G, Long W, Xue Z, et al. Accelerated dysbiosis of gut microbiota during aggravation of DSS-induced colitis by a butyrate-producing bacterium. Sci Rep. 2016;6:27572.CrossRefPubMedPubMedCentral
20.
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–8.CrossRefPubMed
21.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.CrossRefPubMedPubMedCentral
22.
Scanlan PD, Shanahan F, Marchesi JR. Culture-independent analysis of desulfovibrios in the human distal colon of healthy, colorectal cancer and polypectomized individuals. FEMS Microbiol Ecol. 2009;69(2):213–21.CrossRefPubMed
23.
Xiao S, Fei N, Pang X, Shen J, Wang L, Zhang B, et al. A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome. FEMS Microbiol Ecol. 2014;87(2):357–67.CrossRefPubMed
24.
Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60.CrossRefPubMed
25.
Baron EJ, Curren M, Henderson G, Jousimies-Somer H, Lee K, Lechowitz K, et al. Bilophila wadsworthia isolates from clinical specimens. J Clin Microbiol. 1992;30(7):1882–4.PubMedPubMedCentral
26.
Finegold S, Summanen P, Hunt Gerardo S, Baron E. Clinical importance of Bilophila wadsworthia. Eur J Clin Microbiol Infect Dis Off Pub Eur Soc Clin Microbiol. 1992;11(11):1058–63.CrossRef
27.
28.
Hentges DJ, Stein AJ, Casey SW, Que JU. Protective role of intestinal flora against infection with Pseudomonas aeruginosa in mice: influence of antibiotics on colonization resistance. Infect Immun. 1985;47(1):118–22.PubMedPubMedCentral
29.
Shen W, Wolf PG, Carbonero F, Zhong W, Reid T, Gaskins HR, et al. Intestinal and systemic inflammatory responses are positively associated with sulfidogenic bacteria abundance in high-fat-fed male C57BL/6J mice. J Nutr. 2014;144(8):1181–7.CrossRefPubMed
30.
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63.CrossRefPubMed
31.
Okur M, Erbey F, Bektas MS, Kaya A, Dogan M, Acar MN, et al. Retrospective clinical and laboratory evaluation of children with brucellosis. Pediatr Int Off J Jpn Pediatr Soc. 2012;54(2):215–8.CrossRef
32.
Wilson S, Vennervald BJ, Kadzo H, Ireri E, Amaganga C, Booth M, et al. Health implications of chronic hepatosplenomegaly in Kenyan school-aged children chronically exposed to malarial infections and Schistosoma mansoni. Trans R Soc Trop Med Hyg. 2010;104(2):110–6.CrossRefPubMedPubMedCentral
33.
Merchant RH, Oswal JS, Bhagwat RV, Karkare J. Clinical profile of HIV infection. Indian Pediatr. 2001;38(3):239–46.PubMed
34.
35.
Malle E, Steinmetz A, Raynes JG. Serum amyloid A (SAA): an acute phase protein and apolipoprotein. Atherosclerosis. 1993;102(2):131–46.CrossRefPubMed
36.
Andersson CX, Gustafson B, Hammarstedt A, Hedjazifar S, Smith U. Inflamed adipose tissue, insulin resistance and vascular injury. Diabetes Metab Res Rev. 2008;24(8):595–603.CrossRefPubMed
37.
Poitou C, Viguerie N, Cancello R, De Matteis R, Cinti S, Stich V, et al. Serum amyloid A: production by human white adipocyte and regulation by obesity and nutrition. Diabetologia. 2005;48(3):519–28.CrossRefPubMed
38.
Lin Y, Rajala MW, Berger JP, Moller DE, Barzilai N, Scherer PE. Hyperglycemia-induced production of acute phase reactants in adipose tissue. J Biol Chem. 2001;276(45):42077–83.CrossRefPubMed
39.
Scheja L, Heese B, Zitzer H, Michael MD, Siesky AM, Pospisil H, et al. Acute-phase serum amyloid A as a marker of insulin resistance in mice. Exp Diabetes Res. 2008;2008:230837.CrossRefPubMedPubMedCentral
40.
Reigstad CS, Lunden GO, Felin J, Backhed F. Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PLoS ONE. 2009;4(6):e5842.CrossRefPubMedPubMedCentral
41.
Johnson BD, Kip KE, Marroquin OC, Ridker PM, Kelsey SF, Shaw LJ, et al. Serum amyloid A as a predictor of coronary artery disease and cardiovascular outcome in women: the National Heart, Lung, and Blood Institute-Sponsored Women’s Ischemia Syndrome Evaluation (WISE). Circulation. 2004;109(6):726–32.CrossRefPubMed
42.
De Oliveira EM, Ascar TP, Silva JC, Sandri S, Migliorini S, Fock RA, et al. Serum amyloid A links endotoxaemia to weight gain and insulin resistance in mice. Diabetologia. 2016;59(8):1760–8.CrossRefPubMed
43.
Hunter CA, Jones SA. IL-6 as a keystone cytokine in health and disease. Nat Immunol. 2015;16(5):448–57.CrossRefPubMed
44.
45.
Burton KJ, Rosikiewicz M, Pimentel G, Butikofer U, Von Ah U, Voirol MJ, et al. Probiotic yogurt and acidified milk similarly reduce postprandial inflammation and both alter the gut microbiota of healthy, young men. Br J Nutr. 2017;117(9):1312–22.CrossRefPubMed
46.
Mosca A, D’alagni M, Del Prete R, De Michele GP, Summanen PH, Finegold SM, et al. Preliminary evidence of endotoxic activity of Bilophila wadsworthia. Anaerobe. 1995;1(1):21–4.CrossRefPubMed
47.
Gerardo SH, Garcia MM, Wexler HM, Finegold SM. Adherence of Bilophila wadsworthia to cultured human embryonic intestinal cells. Anaerobe. 1998;4(1):19–27.CrossRefPubMed
48.
Da Silva SM, Venceslau SS, Fernandes CL, Valente FM, Pereira IA. Hydrogen as an energy source for the human pathogen Bilophila wadsworthia. Antonie Van Leeuwenhoek. 2008;93(4):381–90.CrossRefPubMed
49.
Blachier F, Davila AM, Mimoun S, Benetti PH, Atanasiu C, Andriamihaja M, et al. Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids. 2010;39(2):335–47.CrossRefPubMed
50.
Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761–72.CrossRefPubMed
51.
52.
Sanz Y, Santacruz A, Gauffin P. Gut microbiota in obesity and metabolic disorders. Proc Nutr Soc. 2010;69(3):434–41.CrossRefPubMed
53.
Derrien M, Collado MC, Ben-Amor K, Salminen S, De Vos WM. The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol. 2008;74(5):1646–8.CrossRefPubMed
Metadata
Title
A human stool-derived Bilophila wadsworthia strain caused systemic inflammation in specific-pathogen-free mice
Authors
Zhou Feng
Wenmin Long
Binhan Hao
Ding Ding
Xiaoqing Ma
Liping Zhao
Xiaoyan Pang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0208-7

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