Skip to main content

Advertisement

SpringerLink
Log in

In vitro Effects of Cellulose Acetate on Fermentation Profiles, the Microbiome, and Gamma-aminobutyric Acid Production in Human Stool Cultures

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Gamma-aminobutyric acid (GABA) is considered as a potential candidate substance that mediates the effects of intestinal bacteria on human mental health. In the present study, we evaluated the effect of water-soluble cellulose acetate (WSCA), a type of cellulose ester, on fermentation and microbial profiles, and GABA production in human stool cultures prepared from fresh feces from volunteers. In addition, the GABA-producing ability of Bacteroides uniformis, which can utilize WSCA, was evaluated in a pure-culture study. All incubations were conducted anaerobically. WSCA supplementation increased (P < 0.05) acetate and propionate production and decreased (P < 0.05) the pH in human fecal cultures. WSCA significantly altered the microbiota, selectively increasing the relative abundance of B. uniformis (P < 0.05). Pure-culture study results revealed that B. uniformis produces GABA, possibly via a glutamate-dependent acid resistance system under low pH conditions. In conclusion, WSCA could be a potential prebiotic material that is fermented by intestinal bacteria and increases short-chain fatty acid and GABA production in the human gut. Bacteroides uniformis might play an important role in both WSCA degradation and GABA production in the intestine.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

All data and material are available with corresponding author.

Code Availability

Not applicable.

Abbreviations

CA:

Cellulose acetate

CCS:

Circular consensus reads

GABA:

Gamma-aminobutyric acid

MM:

Minimal medium

PCoA:

Principal coordinate analysis

qPCR:

Quantitative real-time PCR

SCFAs:

Short-chain fatty acids

WSCA:

Water-soluble cellulose acetate

References

  1. Whitman W, Coleman D, Wiebe W (2005) Prokaryotes: the unseen majority. Brain Res 95:6578–6583. https://doi.org/10.1073/pnas.95.12.6578

    Article  Google Scholar 

  2. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920. https://doi.org/10.1126/science.1104816

    Article  CAS  PubMed  Google Scholar 

  3. Illiano P, Brambilla R, Parolini C (2020) The mutual interplay of gut microbiota, diet and human disease. FEBS J 287:833–855. https://doi.org/10.1111/febs.15217

    Article  CAS  PubMed  Google Scholar 

  4. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, Cameron J, Grosse J, Reimann F, Gribble FM (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 61:364–371. https://doi.org/10.2337/db11-1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ben-Shlomo S, Zvibel I, Shnell M, Shlomai A, Chepurko E, Halpern Z, Barzilai N, Oren R, Fishman S (2011) Glucagon-like peptide-1 reduces hepatic lipogenesis via activation of AMP-activated protein kinase. J Hepatol 54:1214–1223. https://doi.org/10.1016/j.jhep.2010.09.032

    Article  CAS  PubMed  Google Scholar 

  6. Puls J, Wilson SA, Hölter D (2011) Degradation of cellulose acetate-based materials: a review. J Polym Environ 19:152–165. https://doi.org/10.1007/s10924-010-0258-0

    Article  CAS  Google Scholar 

  7. Yamada H, Watabe Y, Suzuki Y, Koike S, Shimamoto S, Kobayashi Y (2021) Chemical and microbial characterization for fermentation of water-soluble cellulose acetate in human stool cultures. J Sci Food Agric 101:2950–2960. https://doi.org/10.1002/jsfa.10927

    Article  CAS  PubMed  Google Scholar 

  8. 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. https://doi.org/10.1021/acs.jafc.8b04093

    Article  CAS  PubMed  Google Scholar 

  9. Roshchina V (2010) Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells, In: Microbial endocrinology. Springer, New York, pp 17–52. https://doi.org/10.1007/2F978-1-4419-5576-0_2

  10. Özoğul F, Kuley E, Özoğul Y, Özoğul İ (2012) The function of lactic acid bacteria on biogenic amines production by food-borne pathogens in arginine decarboxylase broth. Food Sci Technol Res 18:795–804. https://doi.org/10.3136/fstr.18.795

    Article  Google Scholar 

  11. Bailey MT, Coe CL (1999) Maternal separaseparation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35:146–155. https://pubmed.ncbi.nlm.nih.gov/10461128/

  12. Dinan TG, Stanton C, Cryan JF (2013) Psychobiotics: a novel class of psychotropic. Biol Psychiatry 74:720–726. https://doi.org/10.1016/j.biopsych.2013.05.001

    Article  CAS  PubMed  Google Scholar 

  13. Sarkar A, Lehto SM, Harty S, Dinan TG, Cryan JF, Burnet PWJ (2016) Psychobiotics and the manipulation of bacteria–gut–brain signals. Trends Neurosci 39:763–781. https://doi.org/10.1016/j.tins.2016.09.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Yunes RA, Poluektova EU, Dyachkova MS, Klimina KM, Kovtun AS, Averina OV, Orlova VS, Danilenko VN (2016) GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota. Anaerobe 42:197–204. https://doi.org/10.1016/j.anaerobe.2016.10.011

    Article  CAS  PubMed  Google Scholar 

  15. Kim YW, Jeong YJ, Kim AY, Son HH, Lee JA, Jung CH, Kim CH, Kim J (2014) Lactobacillus brevis strains from fermented Aloe vera survive gastroduodenal environment and suppress common food borne enteropathogens. PLoS ONE 9:1–10. https://doi.org/10.1371/journal.pone.0090866

    Article  CAS  Google Scholar 

  16. Pokusaeva K, Johnson C, Luk B, Uribe G, Fu Y, Oezguen N, Matsunami RK, Lugo M, Major A, Mori-Akiyama Y, Hollister EB, Dann SM, Shi XZ, Engler DA, Savidge T, Versalovic J (2017) GABA-producing Bifidobacterium dentium modulates visceral sensitivity in the intestine. Neurogastroenterol Motil 29:e12904. https://doi.org/10.1111/nmo.12904

    Article  CAS  PubMed  Google Scholar 

  17. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 108:16050–16055. https://doi.org/10.1073/pnas.1102999108

    Article  PubMed  PubMed Central  Google Scholar 

  18. 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 9:1–15. https://doi.org/10.1038/s41598-019-51781-x

    Article  CAS  Google Scholar 

  19. Yunes RA, Poluektova EU, Vasileva EV, Odorskaya MV, Marsova MV, Kovalev GI, Danilenko VN (2020) A multi-strain potential probiotic formulation of GABA-producing Lactobacillus plantarum 90sk and Bifidobacterium adolescentis 150 with antidepressant effects. Probiotics Antimicrob Proteins 12:973–979. https://doi.org/10.1007/s12602-019-09601-1

    Article  CAS  PubMed  Google Scholar 

  20. Strandwitz P, Kim KH, Terekhova D, Liu JK, Sharma A, Levering J, McDonald D, Dietrich D, Ramadhar TR, Lekbua A, Mroue N, Liston C, Stewart EJ, Dubin MJ, Zengler K, Knight R, Gilbert JA, Clardy J, Lewis K (2019) GABA-modulating bacteria of the human gut microbiota. Nat Microbiol 4:396–403. https://doi.org/10.1038/s41564-018-0307-3

    Article  CAS  PubMed  Google Scholar 

  21. Camacho LF, Silva TE, Palma MNN, Assunção AS, Rodrigues JP, Silva CELF, Detmann E (2019) Evaluation of buffer solutions and urea addition for estimating the in vitro digestibility of feeds. J Anim Sci 97:922–931. https://doi.org/10.1093/jas/sky464

    Article  PubMed  Google Scholar 

  22. Martens EC, Chiang HC, Gordon JI (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4:447–457. https://doi.org/10.1016/j.chom.2008.09.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nocek E, Hart SP, Polan CE (1987) Rumen ammonia concentration as influenced bystorage time, freezing and thawing, acid preservative, and method of ammonia determination. J Dairy Sci 70:601–607. https://doi.org/10.3168/jds.S0022-0302(87)80047-4

    Article  CAS  Google Scholar 

  24. Matsumoto K, Takada T, Yuki N, Kawakami K, Sakai T, Nomoto K, Kimura K, Matsumoto K, Iino H. (2004) Effect of transgalactosylated oligosaccharides mixture (N-GOS) on human intestinal microflora. J Intest Microbiol 18:25–35. https://doi.org/10.11209/2Fjim.18.25

  25. Walstra P, Claudi-Magnussen C, Chevillon P, Von SG, Diestre A, Matthews KR, Homer DB, Bonneau M (1999) An international study on the importance of androstenone and skatole for boar taint: levels of androstenone and skatole by country and season. Livest Prod Sci 62:15–28. https://doi.org/10.1016/S0301-6226(99)00054-8

    Article  Google Scholar 

  26. Yu Z, Morrison M (2004) Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36:808–812. https://doi.org/10.2144/04365st04

    Article  CAS  PubMed  Google Scholar 

  27. Nygaard AB, Tunsjø HS, Meisal R, Charnock C (2020) A preliminary study on the potential of Nanopore MinION and Illumina MiSeq 16S rRNA gene sequencing to characterize building-dust microbiomes. Sci Rep 10:3209. https://doi.org/10.1038/s41598-020-59771-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700. https://doi.org/10.1128/aem.59.3.695-700.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68:5445–5451. https://doi.org/10.1128/AEM.68.11.5445-5451.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tong J, Liu C, Summanen P, Xu H, Finegold SM (2011) Application of quantitative real-time PCR for rapid identification of Bacteroides fragilis group and related organisms in human wound samples. Anaerobe 17:64–68. https://doi.org/10.1016/j.anaerobe.2011.03.004

    Article  CAS  PubMed  Google Scholar 

  31. Altaner C, Saake B, Tenkanen M, Eyzaguirre J, Faulds CB, Biely P, Viikari L, Siika-aho M, Puls J (2003) Regioselective deacetylation of cellulose acetates by acetyl xylan esterases of different CE-families. J Biotechnol 105:95–104. https://doi.org/10.1016/s0168-1656(03)00187-1

    Article  CAS  PubMed  Google Scholar 

  32. Moriyoshi K, Yamanaka H, Ohmoto T, Ohe T, Sakai K (2005) Mode of action on deacetylation of acetylated methyl glycoside by cellulose acetate esterase from Neisseria sicca SB. Biosci Biotechnol Biochem 69:1292–1299. https://doi.org/10.1271/bbb.69.1292

    Article  CAS  PubMed  Google Scholar 

  33. Macfarlane GT, Allison C (1986) Utilisation of protein by human gut bacteria. FEMS Microbiol Lett 38:19–24. https://doi.org/10.1111/j.1574-6968.1986.tb01934.x

    Article  CAS  Google Scholar 

  34. Macfarlane GT, Gibson GR, Beatty E, Cummings JH (1992) Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiol Lett 101:81–88. https://doi.org/10.1111/j.1574-6968.1992.tb05764.x

    Article  CAS  Google Scholar 

  35. Smith EA, Macfarlane GT (1997) Dissimilatory amino acid metabolism in human colonic bacteria. Anaerobe 3:327–337. https://doi.org/10.1006/anae.1997.0121

    Article  CAS  PubMed  Google Scholar 

  36. Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, Anastasovska J, Ghourab S, Hankir M, Zhang S, Carling D, Swann JR, Gibson G, Viardot A, Morrison D, Louise Thomas E, Bell JD (2014) The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 5:1–11. https://doi.org/10.1038/ncomms4611

    Article  CAS  Google Scholar 

  37. Shawcross DL (2015) Is it time to target gut dysbiosis and immune dysfunction in the therapy of hepatic encephalopathy? Expert Rev Gastroenterol Hepatol 9:539–542. https://doi.org/10.1586/17474124.2015.1035257

    Article  CAS  PubMed  Google Scholar 

  38. Hung SC, Kuo KL, Wu CC, Tarng DC (2017) Indoxyl sulfate: a novel cardiovascular risk factor in chronic kidney disease. J Am Heart Assoc 6:1–8. https://doi.org/10.1161/JAHA.116.005022

    Article  Google Scholar 

  39. Kurata K, Kawahara H, Nishimura K, Jisaka M, Yokota K, Shimizu H (2019) Skatole regulates intestinal epithelial cellular functions through activating aryl hydrocarbon receptors and p38. Biochem Biophys Res Commun 510:649–655. https://doi.org/10.1016/j.bbrc.2019.01.122

    Article  CAS  PubMed  Google Scholar 

  40. Vera-Ponce de León A, Jahnes BC, Duan J, Camuy-Vélez LA, Sabree ZL (2020) Cultivable, host-specific Bacteroidetes symbionts exhibit diverse polysaccharolytic strategies. Appl Environ Microbiol 86:e00091–20. https://doi.org/10.1128/2FAEM.00091-20

  41. Rôças IN, Siqueira JF (2006) Characterization of Dialister species in infected root canals. J Endod 32:1057–1061. https://doi.org/10.1016/j.joen.2006.04.010

    Article  PubMed  Google Scholar 

  42. Morotomi M, Nagai F, Sakon H, Tanaka R (2008) Dialister succinatiphilus sp. nov. and Barnesiella intestinihominis sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 58:2716–2720. https://doi.org/10.1099/ijs.0.2008/000810-0

    Article  CAS  PubMed  Google Scholar 

  43. Laverde Gomez JA, Mukhopadhya I, Duncan SH, Louis P, Shaw S, Collie-Duguid E, Crost E, Juge N, Flint HJ (2019) Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria. Environ Microbiol 21:259–271. https://doi.org/10.1111/1462-2920.14454

    Article  CAS  PubMed  Google Scholar 

  44. Lin J, In Soo Lee, Frey J, Slonczewski JL, Foster JW (1995) Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177:4097–4104. https://doi.org/10.1128/2Fjb.177.14.4097-4104.1995

  45. Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C (2012) γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 113:411–417. https://doi.org/10.1111/j.1365-2672.2012.05344.x

    Article  CAS  PubMed  Google Scholar 

  46. Otaru N, Ye K, Mujezinovic D, Berchtold L, Constancias F, Cornejo FA, Krzystek A, de Wouters T, Braegger C, Lacroix C, Pugin B (2021) GABA production by human intestinal Bacteroides spp.: prevalence, regulation, and role in acid stress tolerance. Front Microbiol 12:656895. https://doi.org/10.3389/fmicb.2021.656895

    Article  PubMed  PubMed Central  Google Scholar 

  47. Cummings JH, Pomare EW, Branch HWJ, Naylor CPE, MacFarlane GT (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221–1227. https://doi.org/10.1136/gut.28.10.1221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sheedy JR, Wettenhall RE, Scanlon D, Gooley PR, Lewis DP, McGregor N, Stapleton DI, Butt HL, DE Meirleir KL. (2009) Increased D-lactic acid intestinal bacteria in patients with chronic fatigue syndrome. In Vivo 23:621–628. https://iv.iiarjournals.org/content/23/4/621.long

  49. Engevik MA, Hickerson A, Shull GE, Worrell RT (2013) Acidic conditions in the NHE2 -/- mouse intestine result in an altered mucosa-associated bacterial population with changes in mucus oligosaccharides. Cell Physiol Biochem 32:111–128. https://doi.org/10.1159/000356632

    Article  CAS  PubMed  Google Scholar 

  50. Cheng LH, Liu YW, Wu CC, Wang S, Tsai YC (2019) Psychobiotics in mental health, neurodegenerative and neurodevelopmental disorders. J Food Drug Anal 27:632–648. https://doi.org/10.1016/j.jfda.2019.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Agriculture, Hokkaido University, Sapporo, Hokkaido, 060-8589, Japan

    Hiroaki Yamada, Hiroto Miura, Yutaka Suzuki, Satoshi Koike & Yasuo Kobayashi

  2. Daicel Corporation, Tokyo Head Office Satellite, Tokyo, 108-0075, Japan

    Shu Shimamoto

Authors
  1. Hiroaki Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroto Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yutaka Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satoshi Koike
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shu Shimamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yasuo Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HY and YK designed this study. HY performed the research, analyzed the data, and wrote the paper; HM assisted the data analysis. HM, YS, SK, SS and YK revised the manuscript.

Corresponding author

Correspondence to Yasuo Kobayashi.

Ethics declarations

Conflict of Interest

Authors disclose that there are no conflicts of interest.

Ethical Approval

The present study was carried out according to the Hokkaido University Guidelines for Animal Experiments (2007) and the Act on Welfare and Management of Animals (2005). The study involving human stool cultures was approved by the Ethics Committee of the Research Faculty of Agriculture, Hokkaido University (approval number: H301210-No.2).

Consent for Publication

Authors Consent for publication.

Consent to Participate

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 6133 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamada, H., Miura, H., Suzuki, Y. et al. In vitro Effects of Cellulose Acetate on Fermentation Profiles, the Microbiome, and Gamma-aminobutyric Acid Production in Human Stool Cultures. Curr Microbiol 80, 284 (2023). https://doi.org/10.1007/s00284-023-03383-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03383-0

Search

Navigation