1887

Abstract

Obesity is a global health concern, affecting individuals of all ages and genders. One promising strategy to combat obesity is by addressing gut microbiota dysbiosis, with probiotics being a reliable intervention. However, single-strain probiotics may not effectively modulate the complex microbial communities in the gut, suggesting the need for multi-strain approaches.

Probiotics are known to benefit gut health; however, the efficacy of single-strain probiotics in modulating gut microbiota is limited. Multi-strain probiotic community (MSPC) may offer a more effective approach for addressing obesity-related gut dysbiosis, but its specific effects on individuals and microbial diversity require further investigation.

This study aimed to evaluate the potential of a dairy-origin MSPC in modulating obesity-related gut microbiota from lean and obese Pakistani volunteers using a simulated CoMiniGut model.

Gut microbiota from lean and obese volunteers were treated with MSPC in a simulated CoMiniGut system. Bacterial counts, microbial diversity (- and β-diversity) and microbial community composition were analysed pre- and post-treatment. The impact of MSPC on specific bacterial genera and microbial metabolites was assessed, with statistical significance determined (≤0.05).

The effect of MSPC was individualized, reducing bacterial counts in lean 1 and lean 2 samples, while significantly increasing bacterial counts in obese 2 and obese 3 samples (≤0.05). MSPC significantly improved -diversity in lean 2, lean 3, obese 2 and obese 3 samples (≤0.05). Proteobacteria decreased in the lean group and increased in the obese group post-MSPC treatment. In the lean group, pathogenic bacteria such as , and were significantly reduced (≤0.05), whereas beneficial bacteria like and increased significantly in the obese group (≤0.05). Among the selected metabolites, only butanoic acid was detected in all tested samples, with MSPC affecting metabolite concentrations and types.

MSPC demonstrated a potential for modulating gut microbiota dysbiosis in both lean and obese individuals, with effects on bacterial counts, microbial diversity and metabolite concentrations. MSPC could serve as a promising option for personalized the modulation of gut microbiota in obesity management.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001936
2024-11-29
2024-12-14
Loading full text...

Full text loading...

References

  1. Parente E, Ricciardi A, Zotta T. The microbiota of dairy milk: a review. Int Dairy J 2020; 107:104714 [View Article]
    [Google Scholar]
  2. Nawaz F. Genomic and Culture Based Microbiological Characterization of Fermented Milk Product Dahi and its Impact on Product Quality, Nutrition and Safety, In Microbiology. Quaid-I-Azam University: Islamabad; 2017 https://www.semanticscholar.org/paper/GENOMIC-AND-CULTURE-BASED-MICROBIOLOGICAL-OF-MILK-Nawaz/89963fd15173c13c8be14dc1285225aa5495e7f5
  3. Nawaz F, Khan MN, Javed A, Ahmed I, Ali N et al. Genomic and functional characterization of Enterococcus mundtii QAUEM2808, isolated from artisanal fermented milk product dahi. Front Microbiol 2019; 10:434 [View Article] [PubMed]
    [Google Scholar]
  4. Paek JK, Lee SY. Can gut microbiota modulation be used as a practical treatment for obesity?. J Obes Metab Syndr 2018; 27:75–77 [View Article] [PubMed]
    [Google Scholar]
  5. Requena T, Song Y, Peláez C, Martínez-Cuesta MC. Modulation and metabolism of obesity-associated microbiota in a dynamic simulator of the human gut microbiota. LWT 2021; 141:110921 [View Article]
    [Google Scholar]
  6. Aslam H, Marx W, Rocks T, Loughman A, Chandrasekaran V et al. The effects of dairy and dairy derivatives on the gut microbiota: a systematic literature review. Gut Microbes 2020; 12:1799533 [View Article] [PubMed]
    [Google Scholar]
  7. Borriello SP, Hammes WP, Holzapfel W, Marteau P, Schrezenmeir J et al. Safety of probiotics that contain lactobacilli or bifidobacteria. Clin Infect Dis 2003; 36:775–780 [View Article] [PubMed]
    [Google Scholar]
  8. Grover S, Rashmi HM, Srivastava AK, Batish VK. Probiotics for human health -new innovations and emerging trends. Gut Pathog 2012; 4:1–14 [View Article] [PubMed]
    [Google Scholar]
  9. Barathikannan K, Chelliah R, Rubab M, Daliri EB-M, Elahi F et al. Gut microbiome modulation based on probiotic application for anti-obesity: a review on efficacy and validation. Microorganisms 2019; 7:456 [View Article] [PubMed]
    [Google Scholar]
  10. Wiciński M, Gębalski J, Gołębiewski J, Malinowski B. Probiotics for the treatment of overweight and obesity in humans-a review of clinical trials. Microorganisms 2020; 8:1148 [View Article] [PubMed]
    [Google Scholar]
  11. Sergaki C, Lagunas B, Lidbury I, Gifford ML, Schäfer P. Challenges and approaches in microbiome research: from fundamental to applied. Front Plant Sci 2018; 9:1205 [View Article] [PubMed]
    [Google Scholar]
  12. Zarrati M, Salehi E, Mofid V, Zadeh-Attar MJH, Nourijelyani K et al. Relationship between probiotic consumption and IL-10 and IL-17 secreted by pbmcs in overweight and obese people. IJAAI 2013404–406
    [Google Scholar]
  13. Mohammadi-Sartang M, Bellissimo N, Totosy de Zepetnek JO, Brett NR, Mazloomi SM et al. The effect of daily fortified yogurt consumption on weight loss in adults with metabolic syndrome: a 10-week randomized controlled trial. Nutr Metab Cardiovasc Dis 2018; 28:565–574 [View Article] [PubMed]
    [Google Scholar]
  14. Szulińska M, Łoniewski I, van Hemert S, Sobieska M, Bogdański P. Dose-dependent effects of multispecies probiotic supplementation on the lipopolysaccharide (LPS) level and cardiometabolic profile in obese postmenopausal women: a 12-week randomized clinical trial. Nutrients 2018; 10:773 [View Article] [PubMed]
    [Google Scholar]
  15. De Lorenzo A, Costacurta M, Merra G, Gualtieri P, Cioccoloni G et al. Can psychobiotics intake modulate psychological profile and body composition of women affected by normal weight obese syndrome and obesity? A double blind randomized clinical trial. J Transl Med 2017; 15:135 [View Article] [PubMed]
    [Google Scholar]
  16. Imran M, Desmasures N, Vernoux J-P. From undefined red smear cheese consortia to minimal model communities both exhibiting similar anti-listerial activity on a cheese-like matrix. Food Microbiol 2010; 27:1095–1103 [View Article] [PubMed]
    [Google Scholar]
  17. Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 2016; 6:71–79 [View Article] [PubMed]
    [Google Scholar]
  18. Dlamini ZC, Langa RLS, Aiyegoro OA, Okoh AI. Safety evaluation and colonisation abilities of four lactic acid bacteria as future probiotics. Probiotics Antimicro Prot 2019; 11:397–402 [View Article]
    [Google Scholar]
  19. Madeeha IR, Ikram A, Imran M. A preliminary insight of correlation between human fecal microbial diversity and blood lipid profile. Int J Food Sci Nutr 2016; 67:865–871 [View Article] [PubMed]
    [Google Scholar]
  20. Hui Y, Tamez-Hidalgo P, Cieplak T, Satessa GD, Kot W et al. Supplementation of a lacto-fermented rapeseed-seaweed blend promotes gut microbial- and gut immune-modulation in weaner piglets. J Anim Sci Biotechnol 2021; 12:85 [View Article] [PubMed]
    [Google Scholar]
  21. Wiese M, Khakimov B, Nielsen S, Sørensen H, van den Berg F et al. CoMiniGut-a small volume in vitro colon model for the screening of gut microbial fermentation processes. PeerJ 2018; 6:e4268 [View Article] [PubMed]
    [Google Scholar]
  22. Tsitko I, Wiik-Miettinen F, Mattila O, Rosa-Sibakov N, Seppänen-Laakso T et al. A small in vitro fermentation model for screening the gut microbiota effects of different fiber preparations. Int J Mol Sci 2019; 20:1925 [View Article] [PubMed]
    [Google Scholar]
  23. Mohd Kamal K, Mahamad Maifiah MH, Abdul Rahim N, Hashim YZHY, Abdullah Sani MS et al. Bacterial metabolomics: sample preparation methods. Biochem Res Int 2022; 2022:9186536 [View Article] [PubMed]
    [Google Scholar]
  24. Krasowska A, Sigler K. How microorganisms use hydrophobicity and what does this mean for human needs?. Front Cell Infect Microbiol 2014; 4:112 [View Article] [PubMed]
    [Google Scholar]
  25. Balakrishna A. In vitro evaluation of adhesion and aggregation abilities of four potential probiotic strains isolated from guppy (Poecilia reticulata). Braz Arch Biol Technol 2013; 56:793–800 [View Article]
    [Google Scholar]
  26. Bhola J, Bhadekar R. Invitro synergistic activity of lactic acid bacteria against multi-drug resistant Staphylococci. BMC Complement Altern Med 2019; 19:70 [View Article] [PubMed]
    [Google Scholar]
  27. Akbarzadeh F, Homayouni A. Dairy probiotic foods and coronary heart disease: a review on mechanism of action. Probiotics InTech 2012121–128
    [Google Scholar]
  28. Mahe MM, Brown NE, Poling HM, Helmrath MA. In Vivo Model of Small Intestine. Organ Regeneration: 3D Stem Cell Culture Manipulation 2017 pp 229–245
    [Google Scholar]
  29. Cook MT, Tzortzis G, Charalampopoulos D, Khutoryanskiy VV. Microencapsulation of probiotics for gastrointestinal delivery. J Control Release 2012; 162:56–67 [View Article] [PubMed]
    [Google Scholar]
  30. Martinsen TC, Bergh K, Waldum HL. Gastric juice: a barrier against infectious diseases. Basic Clin Pharma Tox 2005; 96:94–102 [View Article]
    [Google Scholar]
  31. Uriot O, Kebouchi M, Lorson E, Galia W, Denis S et al. Identification of Streptococcus thermophilus genes specifically expressed under simulated human digestive conditions using R-IVET technology. Microorganisms 2021; 9:1113 [View Article] [PubMed]
    [Google Scholar]
  32. Nigam Y, Knight J, Williams N. Gastrointestinal tract 4: anatomy and role of the jejunum and ileum. Nurs times 2019; 115:43–46
    [Google Scholar]
  33. Jacobsen NMY, Nedergaard HB, Kock A, Caglayan I, Laursen MM et al. Development of gastro-resistant coated probiotic granulates and evaluation of viability and release during simulated upper gastrointestinal transit. LWT 2021; 144:111174 [View Article]
    [Google Scholar]
  34. Matouskova P, Hoova J, Rysavka P, Marova I. Stress effect of food matrices on viability of probiotic cells during model digestion. Microorganisms 2021; 9:1625 [View Article] [PubMed]
    [Google Scholar]
  35. Han S, Lu Y, Xie J, Fei Y, Zheng G et al. Probiotic gastrointestinal transit and colonization after oral administration: a Long journey. Front Cell Infect Microbiol 2021; 11:609722 [View Article] [PubMed]
    [Google Scholar]
  36. Yao M, Xie J, Du H, McClements DJ, Xiao H et al. Progress in microencapsulation of probiotics: a review. Comp Rev Food Sci Food Safe 2020; 19:857–874 [View Article]
    [Google Scholar]
  37. Papadimitriou K, Alegría Á, Bron PA, de Angelis M, Gobbetti M et al. Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 2016; 80:837–890 [View Article] [PubMed]
    [Google Scholar]
  38. Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA. An in vitro study of the effect of probiotics, prebiotics and synbiotics on the elderly faecal microbiota. Anaerobe 2014; 27:50–55 [View Article] [PubMed]
    [Google Scholar]
  39. Joseph N, Clayton JB, Hoops SL, Linhardt CA, Mohd Hashim A et al. Alteration of the gut microbiome in normal and overweight school children from selangor with Lactobacillus fermented milk administration. Evol Bioinform Online 2020; 16:1176934320965943 [View Article]
    [Google Scholar]
  40. Zhu L, Liu W, Alkhouri R, Baker RD, Bard JE et al. Structural changes in the gut microbiome of constipated patients. Physiol Genomics 2014; 46:679–686 [View Article] [PubMed]
    [Google Scholar]
  41. Noh C-K, Kim BS, Hong G, Cheong JY, Lee KJ. Effects of the administration of probiotics on fecal microbiota diversity and composition in healthy individuals. J Neurogastroenterol Motil 2018; 24:452–459 [View Article] [PubMed]
    [Google Scholar]
  42. Stojanov S, Berlec A, Štrukelj B. The influence of probiotics on the firmicutes/bacteroidetes ratio in the treatment of obesity and inflammatory bowel disease. Microorganisms 2020; 8:1715 [View Article] [PubMed]
    [Google Scholar]
  43. Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. Biomed Res Int 2017; 2017:9351507 [View Article] [PubMed]
    [Google Scholar]
  44. Huang Y, Shi X, Li Z, Shen Y, Shi X et al. Possible association of Firmicutes in the gut microbiota of patients with major depressive disorder. Neuropsychiatr Dis Treat 2018; 14:3329–3337 [View Article] [PubMed]
    [Google Scholar]
  45. Sanchis-Chordà J, Del Pulgar EMG, Carrasco-Luna J, Benítez-Páez A, Sanz Y et al. Bifidobacterium pseudocatenulatum CECT 7765 supplementation improves inflammatory status in insulin-resistant obese children. Eur J Nutr 2019; 58:2789–2800 [View Article] [PubMed]
    [Google Scholar]
  46. Karlsson Videhult F, Andersson Y, Öhlund I, Stenlund H, Hernell O et al. Impact of probiotics during weaning on the metabolic and inflammatory profile: follow-up at school age. Int J Food Sci Nutr 2015; 66:686–691 [View Article] [PubMed]
    [Google Scholar]
  47. Callaway LK, McIntyre HD, Barrett HL, Foxcroft K, Tremellen A et al. Probiotics for the prevention of gestational diabetes mellitus in overweight and obese women: findings from the SPRING double-blind randomized controlled trial. Diabetes Care 2019; 42:364–371 [View Article] [PubMed]
    [Google Scholar]
  48. Weaver JA, Beverly BEJ, Keshava N, Mudipalli A, Arzuaga X et al. Hazards of diethyl phthalate (DEP) exposure: a systematic review of animal toxicology studies. Environ Int 2020; 145:105848 [View Article] [PubMed]
    [Google Scholar]
  49. Le Poul E, Loison C, Struyf S, Springael J-Y, Lannoy V et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 2003; 278:25481–25489 [View Article] [PubMed]
    [Google Scholar]
  50. Yamashiro K, Tanaka R, Urabe T, Ueno Y, Yamashiro Y et al. Gut dysbiosis is associated with metabolism and systemic inflammation in patients with ischemic stroke. PLoS One 2017; 12:e0171521 [View Article] [PubMed]
    [Google Scholar]
  51. Musini A, Rao JP, Giri A. Phytochemicals of Salacia oblonga responsible for free radical scavenging and antiproliferative activity against breast cancer cell lines (MDA-MB-231). Physiol Mol Biol Plants 2015; 21:583–590 [View Article]
    [Google Scholar]
  52. Trivedi DK, Sinclair E, Xu Y, Sarkar D, Walton-Doyle C et al. Discovery of volatile biomarkers of Parkinson’s disease from sebum. ACS Cent Sci 2019; 5:599–606 [View Article] [PubMed]
    [Google Scholar]
  53. McGeer PL, McGeer EG. Inflammation and neurodegeneration in Parkinson’s disease. Parkinsonism Relat Disord 2004; 10:S3–S7 [View Article]
    [Google Scholar]
  54. Aparna V, Dileep KV, Mandal PK, Karthe P, Sadasivan C et al. Anti-inflammatory property of n-hexadecanoic acid: structural evidence and kinetic assessment. Chem Biol Drug Des 2012; 80:434–439 [View Article] [PubMed]
    [Google Scholar]
  55. Tasdemir SS, Sanlier N. An insight into the anticancer effects of fermented foods: a review. J Funct Foods 2020; 75:104281 [View Article]
    [Google Scholar]
  56. Todesco T, Rao AV, Bosello O, Jenkins DJ. Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. Am J Clin Nutr 1991; 54:860–865 [View Article] [PubMed]
    [Google Scholar]
  57. Angelini G, Foti C, Rigano L, Vena GA. 3‐Dimethylaminopropylamine: a key substance in contact allergy to cocamidopropylbetaine?. Contact Dermatitis 1995; 32:96–99 [View Article]
    [Google Scholar]
  58. Valdes DS, So D, Gill PA, Kellow NJ. Effect of dietary acetic acid supplementation on plasma glucose, lipid profiles, and body mass index in human adults: a systematic review and meta-analysis. J Acad Nutr Diet 2021; 121:895–914 [View Article] [PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001936
Loading
/content/journal/jmm/10.1099/jmm.0.001936
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error