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Probiotic Potential of Bacillus licheniformis and Bacillus pumilus Isolated from Tibetan Yaks, China

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Abstract

Yak (Bos grunniens) inhabit an oxygen-deficient environment at the altitude of 3000 m on the Tibetan Plateau, with a distinctive gut micro-ecosystem. This study evaluated the probiotic potential and physiological property of Bacillus licheniformis and Bacillus pumilus isolated from the gut of yaks. Four strains, two Bacillus licheniformis (named D1 and D2) and two Bacillus pumilus (named X1 and X2), were isolated and identified by 16S rRNA sequencing. All strains had potential antibacterial ability against three indicator pathogens: Escherichia coli C83902, Staphylococcus aureus BNCC186335, and Salmonella enteritidis NTNC13349. The antioxidant activity test showed that D2 sample showed the highest antioxidant activity. Furthermore, all four strains had a higher hydrophobicity, auto-aggregation, acid tolerance, bile tolerance, and antibiotic sensitivity, which all contribute to their survival in the gastrointestinal tract and clinical utility. The animal experimentation (40 KM mice, equally divided into five groups of eight mice each) showed that the strain supplementation not only increased daily weight gain and reduced feed conversion ratio, but also increased the length of the jejunum villi and the value of the V/C (Villi/Crypt). In conclusion, this is the first study demonstrated the probiotic potential of Bacillus licheniformis and Bacillus pumilus isolated from yaks, providing a theoretical basis for the clinical application and development of new feed additives.

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References

  1. Lederberg J (2001) Biological warfare. Emerg Infect Dis 7:1071–1072. https://doi.org/10.3201/eid0706.010636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Milani C, Duranti S, Bottacini F et al (2017) The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiol Mol Biol Rev 81:e00036-17. https://doi.org/10.1128/mmbr.00036-17

    Article  PubMed  PubMed Central  Google Scholar 

  3. Strandwitz P (2018) Neurotransmitter modulation by the gut microbiota. Brain Res 1693:128–133. https://doi.org/10.1016/j.brainres.2018.03.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Quigley EMM (2017) Microbiota-brain-gut axis and neurodegenerative diseases. Curr Neurol Neurosci Rep 17:94. https://doi.org/10.1007/s11910-017-0802-6

    Article  PubMed  Google Scholar 

  5. Nishida A, Inoue R, Inatomi O et al (2018) Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 11:1-10. https://doi.org/10.1007/s12328-017-0813-5

    Article  PubMed  Google Scholar 

  6. Mangiola F, Nicoletti A, Gasbarrini A, Ponziani FR (2018) Gut microbiota and aging. Eur Rev Med Pharmacol Sci 22:7404–7413. https://doi.org/10.26355/eurrev-201811-16280

  7. Hill C, Guarner F, Reid G et al (2014) Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  8. Mörkl S, Butler MI, Holl A et al (2020) Probiotics and the microbiota-gut-brain axis: focus on psychiatry. Curr Nutr Rep 9:171–182. https://doi.org/10.1007/s13668-020-00313-5

    Article  PubMed  PubMed Central  Google Scholar 

  9. Yi Y, Zhang Z, Zhao F et al (2018) Probiotic potential of Bacillus velezensis JW: antimicrobial activity against fish pathogenic bacteria and immune enhancement effects on Carassius auratus. Fish Shellfish Immunol 78:322–330. https://doi.org/10.1016/j.fsi.2018.04.055

    Article  CAS  PubMed  Google Scholar 

  10. Dimidi E, Christodoulides S, Scott SM, Whelan K (2017) Mechanisms of action of probiotics and the gastrointestinal microbiota on gut motility and constipation. Adv Nutr 8:484–494. https://doi.org/10.3945/an.116.014407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Abraham BP, Quigley EMM (2017) Probiotics in Inflammatory bowel disease. Gastroenterol Clin North Am 46:769–782. https://doi.org/10.1016/j.gtc.2017.08.003

    Article  PubMed  Google Scholar 

  12. Yang G, Shen K, Yu R et al (2020) Probiotic (Bacillus cereus) enhanced growth of Pengze crucian carp concurrent with modulating the antioxidant defense response and exerting beneficial impacts on inflammatory response via Nrf2 activation. Aquaculture 529:735691. https://doi.org/10.1016/j.aquaculture.2020.735691

    Article  Google Scholar 

  13. Anderson ER, Glasier A (2000) Emergency contraception. Infertil Reprod Med Clin North Am 11:705–713. https://doi.org/10.1002/14651858

    Article  CAS  Google Scholar 

  14. Durchschein F, Petritsch W, Hammer HF (2016) Diet therapy for inflammatory bowel diseases: the established and the new. World J Gastroenterol 22:2179–2194. https://doi.org/10.3748/wjg.v22.i7.2179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bajramagic S, Hodzic E, Mulabdic A et al (2019) Usage of probiotics and its clinical significance at surgically treated patients sufferig from colorectal carcinoma. Med Arch (Sarajevo, Bosnia Herzegovina) 73:316–320. https://doi.org/10.5455/medarh.2019.73.316-320

    Article  Google Scholar 

  16. Li K, Luo H, Mehmood K et al (2019) Sarcosporidiosis: an emerging disease in yaks (Bos grunniens) on the Qinghai Tibetan Plateau (QTP), China. Acta Parasitol 64:246–250. https://doi.org/10.2478/s11686-019-00032-0

    Article  PubMed  Google Scholar 

  17. Gao X, Zhang L, Tong X et al (2020) Epidemiological survey of fasciolosis in yaks and sheep living on the Qinghai-Tibet plateau. China Acta Trop 201:105212. https://doi.org/10.1016/j.actatropica.2019.105212

    Article  PubMed  Google Scholar 

  18. Zhang XX, Feng SY, Ma JG et al (2017) Seroprevalence and risk factors of fascioliasis in yaks, bos grunniens, from three counties of Gansu Province, China. Korean J Parasitol 55:89–93. https://doi.org/10.3347/kjp.2017.55.1.89

    Article  PubMed  PubMed Central  Google Scholar 

  19. Mekonnen SA, Merenstein D, Fraser CM, Marco ML (2020) Molecular mechanisms of probiotic prevention of antibiotic-associated diarrhea. Curr Opin Biotechnol 61:226–234. https://doi.org/10.1016/j.copbio.2020.01.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Li A, Wang Y, Pei L et al (2019) Influence of dietary supplementation with Bacillus velezensis on intestinal microbial diversity of mice. Microb Pathog 136:103671. https://doi.org/10.1016/j.micpath.2019.103671

    Article  PubMed  PubMed Central  Google Scholar 

  21. Qi X, Zhang Q, He Y et al (2019) The transcriptomic landscape of Yaks reveals molecular pathways for high altitude adaptation. Genome Biol Evol 11:72–85. https://doi.org/10.1093/gbe/evy264

    Article  CAS  PubMed  Google Scholar 

  22. Li A, Wang Y, Suolang S et al (2019) Isolation and identification of potential bacillus probiotics from free ranging yaks of Tibetan Plateau, China. Pak Vet J 39:377–382. https://doi.org/10.29261/pakvetj/2019.032

    Article  CAS  Google Scholar 

  23. Zhang J, Li G, Zhang G et al (2021) Performance evaluation of the gradient diffusion strip method and disk diffusion method for ceftazidime–avibactam against Enterobacterales and Pseudomonas aeruginosa: a dual-center study. Front Microbiol 12:710526. https://doi.org/10.3389/fmicb.2021.710526

    Article  PubMed  PubMed Central  Google Scholar 

  24. Dec M, Urban-Chmiel R, Stȩpień-Pyśniak D, Wernicki A (2017) Assessment of antibiotic susceptibility in Lactobacillus isolates from chickens. Gut Pathog 9:54. https://doi.org/10.1186/s13099-017-0203-z

    Article  PubMed  PubMed Central  Google Scholar 

  25. Si J, Wang Z, Wang Z, Li H (2012) Sequencing-based detection of drug-resistant Mycobacterium tuberculosis in patients with spinal tuberculosis. Arch Orthop Trauma Surg 132:941–945. https://doi.org/10.1007/s00402-012-1506-7

    Article  PubMed  Google Scholar 

  26. Dutka-Malen S, Evers S, Courvalin P (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 33:24–27. https://doi.org/10.1128/jcm.33.1.24-27.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ramos-Trujillo E, Pérez-Roth E, Méndez-Alvarez S, Claverie-Martín F (2003) Multiplex PCR for simultaneous detection of enterococcal genes vanA and vanB and staphylococcal genes mecA, ileS-2 and femB. Int Microbiol 6:113–115. https://doi.org/10.1007/s10123-003-0118-z

    Article  CAS  PubMed  Google Scholar 

  28. Qin S, Huang Z, Wang Y et al (2021) Probiotic potential of Lactobacillus isolated from horses and its therapeutic effect on DSS-induced colitis in mice. Microb Pathog 165:105216. https://doi.org/10.1016/j.micpath.2021.105216

    Article  PubMed  Google Scholar 

  29. Chen F, Huang G, Yang Z, Hou Y (2019) Antioxidant activity of Momordica charantia polysaccharide and its derivatives. Int J Biol Macromol 138:673–680. https://doi.org/10.1016/j.ijbiomac.2019.07.129

    Article  CAS  PubMed  Google Scholar 

  30. Talib N, Mohamad NE, Yeap SK et al (2019) Isolation and characterization of Lactobacillus spp. from kefir samples in Malaysia. Molecules 24:2606. https://doi.org/10.3390/molecules24142606

  31. Angelova PR, Horrocks MH, Klenerman D et al (2015) Lipid peroxidation is essential for α-synuclein-induced cell death. J Neurochem 133:582–589. https://doi.org/10.1111/jnc.13024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Elias RJ, Kellerby SS, Decker EA (2008) Antioxidant activity of proteins and peptides. Crit Rev Food Sci Nutr 48:430–441. https://doi.org/10.1080/10408390701425615

    Article  CAS  PubMed  Google Scholar 

  33. Zeng Z, He X, Li F et al (2021) Probiotic properties of Bacillus proteolyticus isolated from Tibetan Yaks, China Front Microbiol 12:649207. https://doi.org/10.3389/fmicb.2021.649207

    Article  PubMed  PubMed Central  Google Scholar 

  34. Xia Y, Qin S, Shen Y (2019) Probiotic potential of Weissella strains isolated from horse feces. Microb Pathog 132:117–123. https://doi.org/10.1016/j.micpath.2019.04.032

    Article  CAS  PubMed  Google Scholar 

  35. Li A, Wang Y, Li Z et al (2019) Probiotics isolated from yaks improves the growth performance, antioxidant activity, and cytokines related to immunity and inflammation in mice. Microb Cell Fact 18:112. https://doi.org/10.1186/s12934-019-1161-6

    Article  PubMed  PubMed Central  Google Scholar 

  36. Metgud R, Astekar MS, Soni A et al (2013) Conventional xylene and xylene-free methods for routine histopathological preparation of tissue sections. Biotech Histochem 88:235–241. https://doi.org/10.3109/10520295.2013.764015

    Article  CAS  PubMed  Google Scholar 

  37. Wayne, P. (2003). National Committee for Clinical Laboratory Standards: Performance Standards for Antimicrobial Susceptibility Testing. NCCLS Doc. M100-S13 (M2 A8), USA.

  38. Gupta V, Garg R (2009) Probiotics. Indian J Med Microbiol 27:202–209. https://doi.org/10.4103/0255-0857.53201

    Article  CAS  PubMed  Google Scholar 

  39. Piqué N, Berlanga M, Miñana-Galbis D (2019) Health benefits of heat-killed (Tyndallized) probiotics: an overview. Int J Mol Sci 20:2534. https://doi.org/10.3390/ijms20102534

    Article  PubMed  PubMed Central  Google Scholar 

  40. Qin J, Li R, Raes J et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65. https://doi.org/10.1038/nature08821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kim SK, Guevarra RB, Kim YT et al (2019) Role of probiotics in human gut microbiome-associated diseases. J Microbiol Biotechnol 29:1335–1340. https://doi.org/10.4014/jmb.1906.06064

    Article  PubMed  Google Scholar 

  42. Jeżewska-Frąckowiak J, Seroczyńska K, Banaszczyk J et al (2018) The promises and risks of probiotic Bacillus species. Acta Biochim Pol 65:509–519. https://doi.org/10.18388/abp.2018_2652

    Article  CAS  PubMed  Google Scholar 

  43. Selma-Royo M, Calatayud Arroyo M, García-Mantrana I et al (2020) Perinatal environment shapes microbiota colonization and infant growth: impact on host response and intestinal function. Microbiome 8:167. https://doi.org/10.1186/s40168-020-00940-8

    Article  PubMed  PubMed Central  Google Scholar 

  44. Wang Y, Li A, Jiang X et al (2018) Probiotic potential of Leuconostoc pseudomesenteroides and Lactobacillus strains isolated from yaks. Front Microbiol 9:2987. https://doi.org/10.3389/fmicb.2018.02987

    Article  PubMed  PubMed Central  Google Scholar 

  45. Jamadagni SN, Godawat R, Garde S (2011) Hydrophobicity of proteins and interfaces: insights from density fluctuations. Annu Rev Chem Biomol Eng 2:147–171. https://doi.org/10.1146/annurev-chembioeng-061010-114156

    Article  CAS  PubMed  Google Scholar 

  46. Lovett CA, Moore BP (1968) Pan- and auto-agglutination in albumin: a serological and immunochemical study of five cases. Immunology 14:357–365

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Kim DH (2018) Gut microbiota-mediated pharmacokinetics of ginseng saponins. J Ginseng Res 42:255–263. https://doi.org/10.1016/j.jgr.2017.04.011

    Article  PubMed  Google Scholar 

  48. Jäger R, Purpura M, Farmer S et al (2018) Probiotic Bacillus coagulans GBI-30, 6086 improves protein absorption and utilization. Probiotics Antimicrob Proteins 10:611–615. https://doi.org/10.1007/s12602-017-9354-y

    Article  CAS  PubMed  Google Scholar 

  49. Filomeni G, De Zio D, Cecconi F (2015) Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ 22:377–388. https://doi.org/10.1038/cdd.2014.150

    Article  CAS  PubMed  Google Scholar 

  50. Rodríguez-Serrano GM, García-Garibay JM, Cruz-Guerrero AE et al (2018) Proteolytic system of streptococcus thermophilus. J Microbiol Biotechnol 28:1581–1588. https://doi.org/10.4014/jmb.1807.07017

    Article  CAS  PubMed  Google Scholar 

  51. Wang K, Zhu Q, Kong X et al (2020) Dietary probiotics or synbiotics supplementation during gestation, lactation, and nursery periods modifies colonic microbiota, antioxidant capacity, and immune function in weaned piglets. Front Vet Sci 7:597832. https://doi.org/10.3389/fvets.2020.597832

    Article  PubMed  PubMed Central  Google Scholar 

  52. Barros RGC, Pereira UC, Andrade JKS et al (2020) In vitro gastrointestinal digestion and probiotics fermentation impact on bioaccessbility of phenolics compounds and antioxidant capacity of some native and exotic fruit residues with potential antidiabetic effects. Food Res Int 136:109614. https://doi.org/10.1016/j.foodres.2020.109614

    Article  PubMed  Google Scholar 

  53. Mohr KI (2016) History of antibiotics research. Curr Top Microbiol Immunol 398:237–272. https://doi.org/10.1007/82_2016_499

    Article  CAS  PubMed  Google Scholar 

  54. Christaki E, Marcou M, Tofarides A (2020) Antimicrobial resistance in bacteria: mechanisms, evolution, and persistence. J Mol Evol 88:26–40. https://doi.org/10.1007/s00239-019-09914-3

    Article  CAS  PubMed  Google Scholar 

  55. Suppasri A, Mas E, Charvet I et al (2013) Building damage characteristics based on surveyed data and fragility curves of the 2011 Great East Japan tsunami. Nat Hazards 66: 319-341. https://doi.org/10.1007/s11069-012-0487-8

  56. Hempel S, Newberry SJ, Maher AR et al (2012) Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA - J Am Med Assoc 307:1959–1969. https://doi.org/10.1001/jama.2012.3507

    Article  CAS  Google Scholar 

  57. Singh VP, Sharma J, Babu S et al (2013) Role of probiotics in health and disease: a review. J Pak Med Assoc 63:253–257 63:253–257. https://doi.org/10.31632/ijalsr.2019v02i02.001

    Article  Google Scholar 

  58. Goodarzi A, Mozafarpoor S, Bodaghabadi M, Mohamadi M (2020) The potential of probiotics for treating acne vulgaris: a review of literature on acne and microbiota. Dermatol Ther 33:e13279. https://doi.org/10.1111/dth.13279

    Article  PubMed  PubMed Central  Google Scholar 

  59. Jedrzejas MJ, Huang WJM (2003) Bacillus species proteins involved in spore formation and degradation: from identification in the genome, to sequence analysis, and determination of function and structure. Crit Rev Biochem Mol Biol 38:173–198. https://doi.org/10.1080/713609234

    Article  CAS  PubMed  Google Scholar 

  60. Dinan TG, Cryan JF (2017) Brain-gut-microbiota axis and mental health. Psychosom Med 79:920–926. https://doi.org/10.1097/PSY.0000000000000519

    Article  PubMed  Google Scholar 

  61. Gomaa EZ (2020) Human gut microbiota/microbiome in health and diseases: a review. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 113:2019–2040. https://doi.org/10.1007/s10482-020-01474-7

    Article  Google Scholar 

  62. Kim HJ, Ingber DE (2013) Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr Biol (United Kingdom) 5:1130–1140. https://doi.org/10.1039/c3ib40126j

    Article  CAS  Google Scholar 

  63. Liu H, Zhang J, Zhang S et al (2014) Oral administration of lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets. J Agric Food Chem 62:860–866. https://doi.org/10.1021/jf403288r

    Article  CAS  PubMed  Google Scholar 

  64. Zheng J, Wittouck S, Salvetti E et al (2020) A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107

    Article  CAS  PubMed  Google Scholar 

  65. He Y, Liu X, Dong Y et al (2021) Enterococcus faecium PNC01 isolated from the intestinal mucosa of chicken as an alternative for antibiotics to reduce feed conversion rate in broiler chickens. Microb Cell Fact 20:122. https://doi.org/10.1186/s12934-021-01609-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Kleessen B, Hartmann L, Blaut M (2003) Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. Br J Nutr 89:597–606. https://doi.org/10.1079/bjn2002827

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by the Chinese Agricultural Research Systems (CARS-37); Key Project of Tibet Autonomous Region (XZ202001ZY0044N), Key Project of Tibet Autonomous Region (XZ202101ZD0002N-05).

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Authors and Affiliations

  1. College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Zhibo Zeng, Jiabin Zhang, Yan Li, Kewei Li, Saisai Gong, Feiran Li, Pengpeng Wang, Mudassar Iqbal, Muhammad Fakhar-e-Alam Kulyar & Jiakui Li

  2. College of Animals Husbandry and Veterinary Medicine, Tibet Agricultural and Animal Husbandry University, Linzhi, Tibet, 860000, People’s Republic of China

    Jiakui Li

  3. Faculty of Veterinary and Animal Sciences, The Islamia University of Bahawalpur, Bahawalpur, 63100, Pakistan

    Mudassar Iqbal

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  1. Zhibo Zeng
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  3. Yan Li
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Contributions

ZZ, and JL conceived and designed the experiments. ZZ, JZ, YL, KL, SG, FL, and PW contributed sample collection and reagent preparation. MFK and MI revised the manuscript. ZZ wrote the manuscript. All authors contributed to the article and approved the submitted version.

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Correspondence to Jiakui Li.

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Ethics Statement

The animal study was authorized by the Ethics Committee of Huazhong Agricultural University (No: 4200695757), and the experimental procedures were based on the state guidelines from the Laboratory Animal Research Center of Hubei province in China.

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Zeng, Z., Zhang, J., Li, Y. et al. Probiotic Potential of Bacillus licheniformis and Bacillus pumilus Isolated from Tibetan Yaks, China. Probiotics & Antimicro. Prot. 14, 579–594 (2022). https://doi.org/10.1007/s12602-022-09939-z

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