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Effects of fermented Aphanizomenon flos-aquae on the caecal microbiome of mice fed a high-sucrose and low-dietary fibre diet

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Abstract

Aphanizomenon flos-aquae, a freshwater cyanobacterium harvested from Upper Klamath Lake, Oregon, USA, is employed as a functional food material. Aphanizomenon flos-aquae can be fermented with Lactobacillus plantarum and Lactococcus lactis subsp. lactis. Here, to determine the dietary effects of A. flos-aquae (AFA) and fermented A. flos-aquae (F-AFA) on the mouse gut microbiome, high-sucrose diet containing no dietary fibre (NF), 5% AFA or 5% F-AFA was administered to ICR mice for 14 days. Compared with those in mice fed the NF, lower body weight gains and epididymal fat pad tissue weights were observed in mice fed the diet containing F-AFA. After feeding, the caecal microbiome was analysed by 16S rRNA (V4) gene amplicon sequencing using the Illumina MiSeq system. Sequences were clustered into operational taxonomic units, with a 97% identity cutoff, using the QIIME2 workflow script and SILVA database. The caecal microbiome alpha diversity was high in mice fed the F-AFA diet. The abundances of Muribaculum- and Alistipes inops-like bacteria belonging to the phylum Bacteroidetes and Ruminococcaceae UCG-014-like bacteria belonging to phylum Firmicutes were higher in the F-AFA group than in the AFA group. Isolation of typical F-AFA-susceptible gut indigenous bacteria and functional studies of the isolates in the presence of F-AFA are warranted to validate the current findings.

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References

  • Al-Qadiri HM, Al-Holy AA, Cavinnato AG, Rasco BA (2008) Detection of sublethal thermal injury in Salmonella enterica serotype Typhimurium and Listeria monocytogenes using fourier transform infrared (FT-IR) spectroscopy. J Food Sci 73:M54–M61

    Article  CAS  PubMed  Google Scholar 

  • Barouei J, Bendiks Z, Martinic A, Mishchuk D, Heeney D, Hsieh Y, Kieffer D, Zaragoza J, Martin R, Slupsky C, Marco M (2017) Microbiota, metabolome, and immune alterations in obese mice fed a high-fat diet containing type 2 resistant starch. Mol Nutr Food Res 61:20170084

    Article  CAS  Google Scholar 

  • Benedetti S, Benvenuti F, Pagliarani S, Francogli S, Scoglio S, Canestrati F (2004) Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sci 75:2353–2362

    Article  CAS  PubMed  Google Scholar 

  • Bo T, Wen J, Zhao Y, Tian S, Zhang X, Wang D (2020) Bifidobacterium pseudolongum reduces triglycerides by modulating gut microbiota in mice fed high-fat food. J Steroid Biochem Mol Biol 198:105602

    Article  CAS  PubMed  Google Scholar 

  • Bunyavanich S, Shen N, Grishin A, Wood R, Burks W, Dawson P (2016) Early-life gut microbiome composition and milk allergy resolution. J Allergy Clin Immunol 138:1122–1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campana R, Martinelli V, Scoglio S, Colombo E, Benedetti S, Baffone W (2017) Influence of Aphanizomenon flos-aquae and two of its extracts on growth ability and antimicrobial properties of Lactobacillus acidophilus DDS-1. LWT-Food Sci Technol 81:291–298

    Article  CAS  Google Scholar 

  • Carmichael WW, Drapeau C, Anderson DM (2000) Harvesting of Aphanizomenon flos-aquae Ralfs ex Born. & Flah. var. flos-aquae (Cyanobacteria) from Klamath Lake for human dietary use. J Appl Phycol 12:585–595

    Article  Google Scholar 

  • Chang S, Cui X, Guo M, Tian Y, Xu W, Huang K, Zhang Y (2017) Insoluble dietary fiber from pear pomace can prevent high-fat diet-induced obesity in rats mainly by improving the structure of the gut microbiota. J Microbiol Biotechnol 27:856–867

    Article  PubMed  CAS  Google Scholar 

  • Cirés S, Ballot A (2016) A review of the phylogeny, ecology and toxin production of bloom-forming Aphanizomenon spp. and related species within the Nostocales (cyanobacteria). Harmful Algae 54:21–23

    Article  PubMed  CAS  Google Scholar 

  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Vama Y, Fishbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563

    Article  CAS  PubMed  Google Scholar 

  • Frazier K, Chang EB (2020) Intersection of the gut microbiome and circadian rhythms in metabolism. Trends Endocrinol Metab 31:25–36

    Article  CAS  PubMed  Google Scholar 

  • Gao R, Zhu C, Li H, Yin M, Pan C, Huang L, Kong C, Wang X, Zhang Y, Qu S, Qin SH (2018) Dysbiosis signatures of gut microbiota along the sequence from healthy, young patients to those with overweight and obesity. Obesity 26:351–361

    Article  CAS  PubMed  Google Scholar 

  • Genda T, Kondo T, Sugiura S, Hino S, Shimamoto S, Nakamura T, Ukita S, Morita T (2018) Bacterial fermentation of water-soluble cellulose acetate raises large-bowel acetate and propionate and decreases plasma cholesterol concentrations in rats. J Agric Food Chem 66:11909–11916

    Article  CAS  PubMed  Google Scholar 

  • Hirota K, Inagaki R, Hamada R, Ishida K, Miyatake Y (2014) Evaluation of a rapid oral bacteria quantification system using dielectrophoresis and the impedance measurement. Biocontrol Sci 19:45–49

    Article  PubMed  Google Scholar 

  • Hussain M, Bonilla-Rosso G, Chung CK, Bariswyl L, Rodriguez MP, Kim BS, Emgel P, Noti M (2019) High dietary fat intake induces a microbiota signature that promotes food allergy. J Clin Immunol 144:157–170

    Article  CAS  Google Scholar 

  • Kim B, Shin J, Guevarra RB, Lee JH, Kim DW, Seol K, Lee JH, Kim HB, Isaacson R (2017) Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 27:2089–2093

    Article  PubMed  Google Scholar 

  • Koliada A, Syzenko G, Moseiko V, Puchkov L, Budovska K, Perederiy V, Gavalko Y, Dorofeyev A, Romanenko M, Tkach S, Sineok L, Lushchak O, Vaiserman A (2017) Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol 17:120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuda T, Yazaki T, Ono M, Takahashi H, Kimura B (2013) In vitro cholesterol-lowering properties of Lactobacillus plantarum AN6 isolated from aji-narezushi. Lett Appl Microbiol 57:187–192

    Article  CAS  PubMed  Google Scholar 

  • Kuda T, Masuko Y, Kawahara M, Kondo S, Nemoto M, Nakata T, Takahashi H, Kimura B (2016) Bile acid-lowering properties of Lactobacillus plantarum Sanriku–SU3 isolated from Japanese surfperch fish. Food Biosci 14:41–46

    Article  CAS  Google Scholar 

  • Kuda T, Yokota Y, Shikano A, Takei M, Takhashi H, Kimura B (2017) Dietary and lifestyle disease indices and caecal microbiota in high fat diet, dietary fibre free diet, or DSS induced IBD models in ICR mice. J Funct Foods 35:605–614

    Article  Google Scholar 

  • Kushak PI, Drapeau C, Van Cott EM, Winter HH (2000) Favorable effects of blue-green algae Aphanizomenon flos-aquae on rat plasma lipids. J Am Nutraceut Assoc 2:59–65

    Google Scholar 

  • Lagkouvardos I, Lesker TR, Hitch TC, Gálvez EJC, Smit N, Neuhaus K, Wang J, Baines JF, Abt B, Stecher B, Overmann J, Strowig T, Clavel T (2019) Sequence and cultivation study of Muribaculaceae reveals novel species, host preference, and functional potential of this yet undescribed family. Microbiome 7:28

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Wang Y, Zhu L, Liu Z, Ye C, Qin S (2020) Inulin with different degrees of polymerization protects against diet-induced endotoxemia and inflammation in association with gut microbiota regulation in mice. Sci Rep 10:978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Fan C, Li P, Lu Y, Chang X, Qi K (2016) Short chain fatty acids prevent high-fat-diet-induced obesity in mice by regulating G protein coupled receptors and gut microbiota. Sci Rep 6:37589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mangin I, Dossou-Yovo F, Lévêque C, Dessoy M, Sawoo O, Suau A, Pochart P (2018) Oral administration of viable Bifidobacterium pseudolongum strain Patronus modified colonic microbiota and increased mucus layer thickness in rat. FEMS Microbiol Ecol 94: fiy177

  • Mitsuoka T (2014) Establishment of intestinal bacteriology. Biosci Microbiota Food Health 33:99–116

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagpal R, Wang S, Ahmadi S, Hayes J, Gagliano J, Subashchandrabose S, Kitzman DW, Becton T, Read R, Yadov H (2018) Human-origin probiotic cocktail increases short-chain fatty acid production via modulation of mice and human gut microbiome. Sci Rep 8:12649

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ni Y, Yang X, Zheng L, Wang Z, Wu L, Jiang J, Yang T, Ma L, Fu Z (2019) Lactobacillus and Bifidobacterium improves physiological function and cognitive ability in aged mice by the regulation of gut microbiota. Mol Nutr Food Res 63:1900603

    Article  CAS  Google Scholar 

  • Patterson E, Ryan PM, Wiley N, Carafa I, Sherwin E, Moloney G, Franciosi E, Mandal R, Wishart DS, Tuohy K, Ross RP, Cryan JF, Dinan TG, Stanton C (2019) Gamma-aminobutyric acid producing lactobacilli positively affect metabolism and depressive like behaviour in a mouse model of metabolic syndrome. Sci Rep 9:16323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Payling L, Fraser K, Loveday SM, Sims I, Roy N, McNabb W (2020) The effects of carbohydrate structure on the composition and functionality of the human gut microbiota. Trends Food Sci Technol 97:233–248

    Article  CAS  Google Scholar 

  • Pereira P, Onodera H, Andorinolo D, Franca S, Araújo F, Lagos N, Oshima Y (2000) Paralytic shellfish toxins in the freshwater cyanobacterium Aphanizomenon flos-aquae, isolated from Montargil reservoir. Portugal Toxicon 38:1689–1702

    Article  CAS  PubMed  Google Scholar 

  • Pugh N, Pasco DS (2001) Characterization of human monocyte activation by a water soluble preparation of Aphanizomenon flos-aquae. Phytomedicine 8:445–453

    Article  CAS  PubMed  Google Scholar 

  • Sharma NK, Tiwari SP, Tripathi K, Rai AK (2011) Sustainability and cyanobacteria (blue-green algae): facts and challenges. J Appl Phycol 23:105–1081

    Article  CAS  Google Scholar 

  • Shikano A, Kuda T, Shinayama J, Toyama A, Ishida Y, Takahashi H, Kimura B (2019) Effects of Lactobacillus plantarum Uruma-SU4 fermented green loofah on plasma lipid levels and gut microbiome of high-fat diet fed mice. Food Res Int 121:817–824

    Article  CAS  PubMed  Google Scholar 

  • Shkoporov AN, Chaplin AV, Khokholova EK, Shcheribakova VA, Motuzova OV, Bozhenko VK, Kafarskaia LI, Efimov BA (2015) Alistipes inops sp. nov. and Coprobacter secundus sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 65:4580–4588

    Article  CAS  PubMed  Google Scholar 

  • Sinclair L, Osman OA, Bertilsson S, Eiler A (2015) Microbial community composition and diversity via 16S rRNA gene amplicons: evaluating the Illumina platform. PLoS One 10:e0116955

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takei M, Kuda T, Fukunaga M, Toyama A, Goto M, Takahashi H, Kimura B (2019) Effects of edible algae on caecal microbiomes of ICR mice fed a high-sucrose and low–dietary fibre diet. J Appl Phycol 31:3969–3978

    Article  CAS  Google Scholar 

  • Takei NM, Kuda T, Taniguchi M, Nakamura S, Takahashi H, Kimura B (2020) Detection and isolation of low molecular weight alginate- and laminaran susceptible gut indigenous bacteria from ICR mice. Carbohydr Polyomers 238:116205

    Article  CAS  Google Scholar 

  • Taniguchi M, Kuda T, Shibayama J, Sasaki T, Michihata T, Takahashi H, Kimura B (2019) In vitro antioxidant, anti-glycation and immunomodulation activities of fermented blue-green algae Aphanizomenon flos-aquae. Mol Biol Rep 46:1775–1786

    Article  CAS  PubMed  Google Scholar 

  • Wang CS, Li WB, Wang HY, Ma YM, Zhao XH, Yang H, Qian JM, Li JN (2018) VSL#3 can prevent ulcerative colitis-associated carcinogenesis in mice. World J Gastroenterol 24:4254–4262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams BA, Mikkeisen D, Flanagan BM, Gidley MJ (2019) “Dietary fibre”: moving beyond the “soluble/insoluble” classification for monogastric nutrition, with an emphasis on humans and pigs. J Animal Sci Biotechnol 10:45

    Article  CAS  Google Scholar 

  • Xia Y, Kuda T, Toyama A, Goto M, Fukunaga M, Takahashi H, Kimura B (2019) Detection and isolation of bacteria affected by dietary cumin, coriander, turmeric, and red chili pepper in the caecum of ICR mice. J Funct Foods 61:103467

    Article  CAS  Google Scholar 

  • Xia Y, Fukunaga M, Kuda T, Goto M, Chiaraluce G, Hoshiba H, Takahashi H, Kimura B (2020) Detection and isolation of protein susceptible indigenous bacteria affected by dietary milk-casein, albumen and soy-protein in the caecum of ICR mice. J Biol Macromol 144:813–820

    Article  CAS  Google Scholar 

  • Yokota Y, Haraguchi Y, Shikano A, Kuda T, Takahashi H, Kimura B (2018) Induction of gut Lactobacillus reuteri in normal ICR mice by oral administration of L. plantarum AN1. J Food Biochem 42:e12589

    Article  CAS  Google Scholar 

  • Zhang L, Liu SY, Zhang J, Zhang JK, Hu C, Liu CX (2016) Respiratory toxicity of cyanobacterial aphantoxins from Aphanizomenon flos-aquae DC-1 in the zebrafish gill. Aquat Toxicol 176:106–115

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Wu W, Li X, Xin X, Liu D (2019) Daily supplementation with fresh Angelica keiskei juice alleviates high-fat diet-induced obesity in mice by modulating gut microbiota composition. Mol Nutr Food Res 63:19000248

    Google Scholar 

  • Zhao L, Lou H, Peng Y, Chen S, Zhang Y, Li X (2019) Comprehensive relationships between gut microbiome and faecal metabolome in individuals with type 2 diabetes and its complications. Endocrine 66:526–537

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Editage (www.editage.com) for the English language editing.

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This work was partially supported by the Towa Foundation for Food Science & Research, Tokyo, Japan.

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Correspondence to Takashi Kuda.

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Animal experiments were performed in accordance with the Fundamental Guidelines for Proper Conduct of Animal Experiments and Related Activities in Academic Research Institutions, under the jurisdiction of the Ministry of Education, Culture, Sports, Science and Technology, Japan. The study protocol was approved by the Animal Experiment Committee of the Tokyo University of Marine Science and Technology (Approval No. H31-5).

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Taniguchi, M., Kuda, T., Takei, M. et al. Effects of fermented Aphanizomenon flos-aquae on the caecal microbiome of mice fed a high-sucrose and low-dietary fibre diet. J Appl Phycol 33, 397–407 (2021). https://doi.org/10.1007/s10811-020-02306-x

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  • DOI: https://doi.org/10.1007/s10811-020-02306-x

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