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Cultivable Butyrate-Producing Bacteria of Elderly Japanese Diagnosed with Alzheimer's Disease

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Cultivable Butyrate-Producing Bacteria of Elderly Japanese Diagnosed with Alzheimer's Disease Journal of Microbiology (2018) Vol. 56 eISSN 1976-3794 DOI 10.1007/s12275-018-8297-7 pISSN 1225-8873 Cultivable butyrate-producing bacteria of elderly Japanese diagnosed with Alzheimer’s disease§ Thi Thuy Tien Nguyen1,2, Yuta Fujimura1, of AD patients. Iyo Mimura3, Yusuke Fujii1, 4 1 Keywords: 16S rRNA gene sequencing, Alzheimer’s disease, Ngoc Luong Nguyen , Kensuke Arakawa , butyrate-producing bacteria, gut microbiota, short-chain and Hidetoshi Morita1* fatty acids 1Graduate School of Environmental and Life Science, Okayama University, Okayama 700-8530, Japan Introduction 2College of Agriculture and Forestry, Hue University, Hue 531940, Vietnam 3Graduate School of Interdisciplinary Information Studies, The University The trillions of microorganisms in the human gut play a of Tokyo 113-0033, Japan 4 key role in the host’s life with many beneficial health effects. College of Science, Hue University, Hue 530000, Vietnam They may promote digestion of foods and absorption of (Received Jun 7, 2018 / Revised Jul 4, 2018 / Accepted Jul 4, 2018) nutrients, produce vitamins, protect the host from oppor- tunistic pathogens, improve the immune system, and main- The group of butyrate-producing bacteria within the human tain the host’s homeostasis of its immune system (Wallace gut microbiome may be associated with positive effects on et al., 2011; Sommer and Backhed, 2013). Within the com- memory improvement, according to previous studies on de- munity of human gut microbiota, the group of butyrate-pro- mentia-associated diseases. Here, fecal samples of four eld- ducing bacteria attracts particular attention because of the erly Japanese diagnosed with Alzheimer’s disease (AD) were specific health-promoting effects they provide to their hosts used to isolate butyrate-producing bacteria. 226 isolates were (Vital et al., 2014). Their major metabolic end-product, bu- randomly picked, their 16S rRNA genes were sequenced, tyrate, is not only a preferred energy source for colonocytes and assigned into sixty OTUs (operational taxonomic units) but also a major contributor to the preservation of intestinal based on BLASTn results. Four isolates with less than 97% epithelial permeability and the protection of the host from homology to known sequences were considered as unique carcinogenic, inflammatory, and oxidative factors (Hamer OTUs of potentially butyrate-producing bacteria. In addi- et al., 2008). Furthermore, butyrate was shown to improve tion, 12 potential butyrate-producing isolates were selected memory function in an Alzheimer’s disease (AD) mouse from the remaining 56 OTUs based on scan-searching against model (Govindarajan et al., 2011). the PubMed and the ScienceDirect databases. Those belonged The characteristics and phylogenetic diversity of butyrate- to the phylum Bacteroidetes and to the clostridial clusters I, producing bacteria in the healthy human gut have been wi- IV, XI, XV, XIVa within the phylum Firmicutes. 15 out of dely investigated (Barcenilla et al., 2000; Pryde et al., 2002; the 16 isolates were indeed able to produce butyrate in culture Hamer et al., 2008; Louis and Flint, 2009; Vital et al., 2014). as determined by high-performance liquid chromatography Butyrate-producing bacteria are extremely difficult to culti- with UV detection. Furthermore, encoding genes for buty- vate due to their obligate anaerobic lifestyle and their requi- rate formation in these bacteria were identified by sequenc- rement for specific nutrients. They are mostly Gram-posi- ing of degenerately primed PCR products and included the tive bacteria, belonging to the phylum of Firmicutes within genes for butyrate kinase (buk), butyryl-CoA: acetate CoA- clostridial clusters IV and XIVa (Barcenilla et al., 2000; Pryde transferase (but), CoA-transferase-related, and propionate et al., 2002; Louis and Flint, 2009; Rivière et al., 2016). How- CoA-transferase. The results showed that eight isolates pos- ever, a metagenomic analysis indicated that a minor portion sessed buk, while five isolates possessed but. The CoA-trans- also included the phyla Actinobacteria, Bacteroidetes, Fuso- fer-related gene was identified as butyryl-CoA:4-hydroxy- bacteria, Proteobacteria, Spirochaetes, and Thermotogae (Vital butyrate CoA transferase (4-hbt) in four strains. No strains et al., 2014). contained the propionate CoA-transferase gene. The bio- The effect of butyrate-producing bacteria on the host-gut chemical and butyrate-producing pathways analyses of bu- microbiota relationship has been investigated in previous tyrate producers presented in this study may help to charac- studies (Vital et al., 2013, 2017; Liu et al., 2015; Bourassa et terize the butyrate-producing bacterial community in the gut al., 2016; Geirnaert et al., 2017; Li et al., 2018). Some of these studies examined butyrate-producing bacteria as probiotic *For correspondence. E-mail: [email protected]; Tel.: in regards to their effects on various diseases (Liu et al., 2015; +81-86-2518343; Fax: +81-86-2518343 Geirnaert et al., 2017). For examples, in patients with inflam- §Supplemental material for this article may be found at matory bowel disease, a reduction in the population of bu- http://www.springerlink.com/content/120956. tyrate-producing bacteria was reported (Ott et al., 2004; Geir- Copyright ⓒ 2018, The Microbiological Society of Korea 2Nguyen et al. naert et al., 2017). In an in vitro system simulating the mu- approved by the Ethics Committee of Okayama University, cus- and lumen-associated microbiota, supplementation of Japan (Approval number 1610-025). Written informed con- either Faecalibacterium prausnitzii or Butyricicoccus pulli- sents were obtained from all participants or their relatives. caecorum 25-3T and a mix of other six butyrate-producers, to the fecal microbiota of Crohn’s disease patients, helped Isolation of bacteria from fecal samples to increase butyrate production and improved epithelial bar- Bacteria from fecal samples were recovered following pre- rier integrity (Geirnaert et al., 2017). Furthermore, in mice vious methods with a minor modification (Morita et al., 2007). suffering from vascular disease, which is the second most All isolation processes were performed under anaerobic con- common dementia-associated disease after AD, the admin- ditions. Therefore, PBS solutions, culture media, and other istration of live Clostridium butyricum to their diet helped materials were kept in an anaerobic chamber up to 24 h be- to regulate gut microbiota by increasing their diversity. This fore use. The anaerobic condition was maintained in the work- was reported to increase butyrate in murine brains, which station by using a tank of anaerobic mixed gas (5% carbon improved memory. Therefore, C. butyricum was considered dioxide, 5% hydrogen, and 90% nitrogen) along with a as a probiotic and it may become an economical therapeutic tank of nitrogen gas. 0.4 ml of each fecal stock sample was option to protect against vascular disease (Liu et al., 2015). recovered in 9.6 ml of PBS solution (Life Technologies) to AD is a progressive neurodegenerative disorder of the cen- generate a 102 dilution of the original fecal material. This tral nervous system, characterized by an onset of dementia solution was thoroughly vortexed and then subsequently di- in the elderly population (aged above 65 years) (Mandell and 8 luted serially in 10-fold steps until a 10 -fold dilution was Green, 2011). It was hypothesized that butyrate or butyrate- obtained. 0.1 ml of each dilution was spread onto blood liver producing bacteria may have positive effects on memory im- (BL) agar medium (Eiken) supplemented with 5% defibri- provement in mouse models of dementia-related diseases nated horse blood and yeast extract, casitone, fatty acids (Govindarajan et al., 2011; Liu et al., 2015). Thus, here we (YCFA) agar medium. All plates were incubated at 37°C for wanted to determine if butyrate-producing bacteria are at 3−7 days in the anaerobic chamber. YCFA medium con- all present or completely absent in the gut microbiota of tained (per 100 ml) 1.5 g agar, 1 g casitone, 0.25 g yeast ex- AD patients. The application of single or mixtures of buty- tract, 0.4 g NaHCO3, 0.1 g cysteine, 0.045 g K2HPO4, 0.045 g rate producers in studies associated with dementia-related KH PO , 0.09 g NaCl, 0.009 g MgSO ·7H O, 0.009 g CaCl , disease (mentioned above) emphasizes the importance of 2 4 4 2 2 0.1 mg resazurin, 1 mg hemin, 1 μg biotin, 1 μg cobalamin, identifying butyrate-producing bacteria and to assess their 3 μg p-aminobenzoic acid, 5 μg folic acid, and 15 μg pyrid- rate of butyrate production. oxamine. SCFAs were added to the medium at final con- In the work presented here, we isolated bacteria from the centrations of 33 mM acetate, 9 mM propionate, and 1 mM feces of four Japanese elders diagnosed with Alzheimer’s each of isobutyrate, isovalerate, and valerate. After sterili- disease. The 16S ribosomal RNA (16S rRNA) gene of each zation by autoclaving, a sterile-filtered solution of vitamins isolate was sequenced. Subsequently, we selected bacteria that and sugars was added to the medium, at a final concentra- might possess butyrate producing ability based on species- tion of 50 mg/L each of thiamine and riboflavin (Duncan et related information available in the literature. We then an- al., 2002) and 2 g/L each of glucose, maltose and cellobiose alyzed them in culture for the production of short-chain fatty (Browne et al., 2016). Single colonies were picked randomly acids (SCFAs), including butyrate, using high-performance and re-streaked on the same media until pure colonies ap- liquid chromatography (HPLC). Furthermore, the presence peared as confirmed by morphology. Each pure isolate was of encoding genes for butyrate production in each strain was used for colony PCR (Polymerase Chain Reaction) and cul- identified. These included butyrate kinase (buk), butyryl- tivated in 5 ml of GAM broth (Gifu Anaerobic Media, Eiken) CoA:acetate CoA-transferase (but), CoA-transferase-related, at 37°C under anaerobic conditions.
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