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A Human Stool-Derived Bilophila Wadsworthia Strain Caused Systemic Inflammation in Specific-Pathogen-Free Mice

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A Human Stool-Derived Bilophila Wadsworthia Strain Caused Systemic Inflammation in Specific-Pathogen-Free Mice Feng et al. Gut Pathog (2017) 9:59 DOI 10.1186/s13099-017-0208-7 Gut Pathogens RESEARCH Open Access A human stool‑derived Bilophila wadsworthia strain caused systemic infammation in specifc‑pathogen‑free mice Zhou Feng, Wenmin Long, Binhan Hao, Ding Ding, Xiaoqing Ma, Liping Zhao and Xiaoyan Pang* Abstract Background: Bilophila wadsworthia is a major member of sulfdogenic bacteria in human gut, it was originally recovered from diferent clinical specimens of intra-abdominal infections and recently was reported potentially linked to diferent chronic metabolic disorders. However, there is still insufcient 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 specifc-pathogen-free mice. Tissue samples and serum were collected after sacrifce. Stool samples were collected at diferent time points to profle the gut microbiota. Results: Bilophila wadsworthia infection resulted in the reduction of body weight and fat mass, apparent hepatos- plenomegaly and elevated serum infammatory factors, including serum amyloid A and interleukin-6, while without signifcant change of the overall gut microbiota structure. Conclusions: These results demonstrated that higher amount of B. wadsworthia caused systemic infammatory response in SPF mice, which adds new evidence to the pathogenicity of this bacterium and implied its potential role to the chronic infammation related metabolic diseases like diabetes. Keywords: Bilophila wadsworthia, Infammation, Hepatosplenomegaly, Gut microbiota, Mice Background and insulin resistance [1]. Another bacterium, Akker- Gut microbiota has been closely linked with many chronic mansia muciniphila has been demonstrated to negatively and refractory diseases such as infammatory bowel dis- correlated with symptoms of obesity and type 2 diabe- ease, colorectal cancer, obesity, diabetes, and even men- tes, and has the potential as a probiotic to reverse high- tal diseases like autism. Te key roles of an increasing fat diet-induced metabolic disorders in mice [2]. Recent number of gut bacteria have been revealed, which her- advances in microbial cultivation and model animal are ald a great progress in our knowledge of the etiology of greatly facilitating our understanding of the fundamen- those diseases and ofer great promise for optimizing tal and ultimate question—”who” does “what” and “how” health and treating diseases in novel ways. For instance, referring to the active roles and mechanisms of human an Enterobacter cloacae strain has been identifed as an gut microbiota [3]. obesity-inducing opportunistic pathogen, whose mono- Bilophila wadsworthia is a sulfte-reducing and hydro- association in germfree mice can recapitulate the obese gen sulfde-producing microbe, which was originally phenotype, including low-grade infammation, adiposity isolated from specimens of peritoneal fuid and tissue of patients with appendicitis [4], while usually difcult to *Correspondence: [email protected] detect in healthy individuals. B. wadsworthia is an obli- State Key Laboratory of Microbial Metabolism, School of Life Sciences gately anaerobic Gram-negative bacillus and can be stim- and Biotechnology, Shanghai Jiao Tong University, 800 Dongchuan Road, Minhang District, Shanghai 200240, China ulated by bile. Since it was named in 1989, there has been © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Feng et al. Gut Pathog (2017) 9:59 Page 2 of 10 limited progress on this bacterium. Till in 2012, research- rifampicin-containing media [15] and was used as the ers began to realize the function of this commensal gut inoculum to mice. bacterium. Devkota reported that a milk-derived satu- rated fat diet induced a bloom of B. wadsworthia in gut Animal trial of SPF mice. And mono-inoculation of this pathobiont Twenty 6-week-old male SPF C57BL/6 mice were pur- in germfree IL10−/− mice fed with milk fat diet can even chased from SLAC Inc. (Shanghai, China). Mice were induce TH1 immune response and colitis development maintained under a regular 12-h light cycle and fed [5]. Tis bacterium was also detected over-represented with normal chow diet ad libitum. After 2 weeks accli- in colonic microbiota of colorectal cancer patients, which mation, animals were randomly assigned to either BW 8 implied its possible role in colorectal carcinogenesis group (daily gavaged with 1 × 10 CFU B. wadsworthia [6]. Tough mounting studies have highlighted the cor- suspended in 100 μL anaerobic PBS solution for 1 week) relations of B. wadsworthia in diferent human diseases or NC group (daily gavaged with an equivalent volume [7–9], especially chronic metabolic diseases, the mecha- of anaerobic PBS solution for 1 week). Body weight and nisms of its pathogenicity are not yet well characterized. food intake were recorded every day. Fresh fecal sam- In the study described here, we obtained an isolate of ples were collected on Day 0, 1, 5 and 7. Living cells of B. wadsworthia from a new-onset LADA (latent autoim- B. wadsworthia were detected by plate counting on ABB mune diabetes in adults) patient. Te objective of this agar supplemented with 10 mM taurine and 100 μg/mL study was to examine the outcome of the infection of this rifampicin. After sacrifce on Day 7, blood, liver, spleen, strain in normal SPF mice, and try to elicit its possible fat and colon were collected. Distal colons were fxed in pathogenicity. 4% paraformaldehyde, embedded in parafn, and stained with hematoxylin/eosin. Te ethical treatment of animals Methods was assured by the Animal Care and Use Committee of Isolation and identifcation of B. wadsworthia the School of Life Sciences and Biotechnology, Shanghai Te B. wadsworthia strain used in this study was isolated Jiao Tong University. from fresh fecal samples of a newly diagnosed LADA 30-year-old female patient. Te study was approved by Enzyme‑linked immunosorbent assay (ELISA) Ethics Committee at Shanghai General Hospital, School Serum concentrations for the following infammation of Medicine, Shanghai Jiao Tong University. Informed markers were determined using ELISA following the consent was signed by the patient. By coincidence, we manufacturer’s instructions: Serum Amyloid A (SAA, had already collected and stored two fecal samples of Tridelta, TP802-M), Lipopolysaccharide Binding Protein this individual 4 years ago when there wasn’t any LADA (LBP, Cell Sciences, CKM043), Interleukin-6 (IL-6, eBio- related symptom developed in this girl. Te DNA abun- science, BMS603HS) and tumor necrosis factor-alpha dance of B. wadsworthia before and after LADA onset (TNF-α, eBioscience, BMS607HS). was detected by Real-time PCR using SYBR Green Supermix (Bio-Rad, 170-8882AP). DNA extraction from Detection of gene expression in the colon fecal samples was conducted as previously described Total RNA from colon was isolated using RNeasy Mini [10]. A B. wadsworthia-specifc PCR primer set targeted Kit (QIAGEN, 74106). 1 μg of RNA was treated with taurine:pyruvate aminotransferase (Tpa) gene was used RNase-free DNase I (Invitrogen, 18068-015). cDNA was to quantify B. wadsworthia in stool [11], and primer set synthesized using SuperScript III First-Strand Synthesis Uni331-F/Uni797-R targeted universal bacterial 16S System for RT-PCR kit (Invitrogen, 18080-051). qPCR rRNA gene was used to quantify total bacteria [12]. was performed using SYBR Green Supermix (Bio-Rad, For B. wadsworthia isolation, a fresh fecal sample was 170-8882AP). Glyceraldehyde-3-phosphate dehydroge- collected and transported into the anaerobic workstation nase (Gapdh) gene was used as an endogenous house- (DG500, DWS, UK) within 5 min after defecation. Bac- keeping gene control. Relative gene expression was teria were isolated using Postgate E medium [13] sup- determined using the 2 −ΔΔCt method [16]. Gene expres- plemented with 0.1% (w/v) bile salt, and then transferred sion levels were normalized to that of NC group. Primer to ABB medium (Anaerobe basal broth) [14] supple- sequences for the targeted mouse genes were presented mented with 10 mM taurine for rapid growth. Identifca- in Table 1 [17]: tion of B. wadsworthia was confrmed by 16S rRNA gene sequencing. Gut microbiota profling To easily detect this B. wadsworthia strain in fecal DNA extraction from fecal samples was conducted as samples of subsequent mice experiment, a spontaneous previously described [18]. A sequencing library of V3– mutant strain for rifampicin resistance was selected on V4 region of the bacterial 16S rRNA gene was prepared Feng et al. Gut Pathog (2017) 9:59 Page 3 of 10 Table 1 Primers used in quantitative PCR assays test was used, depending on whether the data were nor- Primers Sequences mally distributed or not. Gapdh-F 5′-GTGTTCCTACCCCCAATGTGT-3′ Results Gapdh-R 5′-ATTGTCATACCAGGAAATGAGCTT-3′ Isolation and identifcation of B. wadsworthia Il6-F 5′-GTTCTCTGGGAAATCGTGGA-3′ Te B. wadsworthia strain was isolated from fresh feces Il6-R 5′-TGTACTCCAGGTAGCTA-3′ of a female volunteer who was newly diagnosed with Tnfα-F 5′-ACGGCATGGATCTCAAAGAC-3′ LADA. We compared the abundance of B. wadsworthia Tnfα-R 5′-AGATAGCAAATCGGCTGACG-3′ in fecal samples of this individual before and after the Tlr4-F 5′-ATGGCATGGCTTACACCACC-3′ onset of LADA. In the acute disease stage, the abundance Tlr4-R 5′-GAGGCCAATTTTGTCTCCACA-3′ of B. wadsworthia was considerably higher than the sam- ple collected 4 years before the diagnosis (1.11 103 vs. 2 × 1.35 × 10 copies/ng fecal DNA). After modifcation of following the manufacturer’s instruction with some tpa gene copy number with 16S rRNA gene copy number, modifcations [19].
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