Abstract
Probiotics are the living and non-pathogenic microbial supplements which, upon administration in adequate quantities, influence the host organism positively by improving gut health and enhancing intestinal mucosal integrity. They suppress potentially pathogenic microorganisms by competing with them for nutrients as well as space for gut adherence. Lactobacillus species are the most commonly used bacteria in the probiotic preparations and studies show that they have cholesterol-lowering effects on the hosts. Lipids are biological molecules that are insoluble in water and bile salts play a major role in their digestion as they are synthesized and conjugated to taurine or glycine in the liver. Bile salt hydrolase deconjugates taurine or glycine from bile salts. Cholesterol metabolism is influenced by the effect of Lactobacillus species on microbial populations as well as overall metabolic activity of human intestinal microflora. Deconjugation of bile salt, concentration of short-chain fatty acids and molar proportion of propionate constitute the major processes by which cholesterol lowering is brought about by Lactobacillus species. This review summarizes the cholesterol-lowering properties of this species. A significant number of Lactobacillus strains have been known to display substantial bile salt hydrolase activities and identifying those strains for use in therapeutic purposes can be a great advancement. Here, this identification is done using phylogenetic relationship for different identified potential probiotic Lactobacillus strains.
Similar content being viewed by others
References
Gupta V, Garg R (2009) Probiotics. Indian J Med Microbiol 27(3):202–209. https://doi.org/10.4103/0255-0857.53201
Harper A, Naghibi MM, Garcha D (2018) The role of bacteria, probiotics and diet in irritable bowel syndrome. Foods 7(2):1–20. https://doi.org/10.3390/foods7020013
Sánchez B, Delgado S, Blanco-Míguez A et al (2017) Probiotics, gut microbiota, and their influence on host health and disease. Mol Nutr Food Res 61:1–10. https://doi.org/10.1002/mnfr.201600240
Markowiak P (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9(1021):1–30. https://doi.org/10.3390/nu9091021
Chumpitazi BP, Shulman RJ (2016) Underlying molecular and cellular mechanisms in childhood irritable bowel syndrome. Mol Cell Pediatr 3(11):1–9. https://doi.org/10.1186/s40348-016-0036-8
Aziz I, Törnblom H, Simrén M et al (2017) Small intestinal bacterial overgrowth as a cause for irritable bowel syndrome. Curr Opin Gastroenterol 33:196–202. https://doi.org/10.1097/MOG.0000000000000348
Lerardi E (2017) Noninvasive molecular analysis of Helicobacter pylori: Is it time for tailored first-line therapy? World J Gastroenterol 23:2453–2458. https://doi.org/10.3748/wjg.v23.i14.2453
Ooi L, Liong M-T (2010) Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int J Mol Sci 11:2499–2522. https://doi.org/10.3390/ijms11062499
Dunne C, O'Mahony L, Murphy L et al (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386S–392S. https://doi.org/10.1093/ajcn/73.2.386s
Begley M, Hill C, Cormac GH et al (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72(3):1729–1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
Malfertheiner P, Megraud F, O'Morain CA et al (2017) European helicobacter and microbiota study group and consensus panel management of Helicobacter pylori infection the Maastricht V/florence consensus report. Gut 66:6–30. https://doi.org/10.1136/gutjnl-2016-312288
Nguyen TDT, Kang JH (2007) Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int J Food Microbiol 113:358–361. https://doi.org/10.1016/j.ijfoodmicro.2006.08.015
Croft JB, Cresanta JL (1988) Cardiovascular risk in parents of children with extreme lipoprotein cholesterol levels: the Bogalusa heart study. South Med J 81(3):341–349. https://doi.org/10.1097/00007611-198803000-00014
Pereira D, McCartney AL et al (2003) An in vitro study of the probiotic potential of a bile-salt-hydrolyzing Lactobacillus fermentum strain, and determination of its cholesterol-lowering properties. Appl Environ Microbiol 69:4743–4752. https://doi.org/10.1128/AEM.69.8.4743-4752.2003
Tsai CC, Lin PP, Hsieh YM et al (2014) Cholesterol-lowering potentials of lactic acid bacteria based on bile-salt hydrolase activity and effect of potent strains on cholesterol metabolism in vitro and in vivo. Sci World J 2014:1–10. https://doi.org/10.1155/2014/690752
Joyce SA, MacSharry J, Casey PG et al (2014) Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. PNAS 111(20):7421–7426. https://doi.org/10.1073/pnas.1323599111
Brian V, Begley M, Hill C et al (2008) Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. PNAS 105(36):13580–13585. https://doi.org/10.1073/pnas.0804437105
Reid G (1999) The scientific basis for probiotic strains of Lactobacillus. Appl Environ Microbiol 65(9):3763–3766
Kumar M, Nagpal R, Kumar R et al (2012) Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diabetes Res 2012:1–14. https://doi.org/10.1155/2012/902917
Bayat A, Azizi-Soleiman F, Heidari-Beni M et al (2016) Effect of Cucurbita ficifolia and probiotic yogurt consumption on blood glucose, lipid profile, and inflammatory marker in type 2 diabetes. Int J Prev Med 7(30):1–5. https://doi.org/10.4103/2008-7802.175455
Hua LM (2016) Type 2 diabetes and probiotics, prebiotics and synbiotics: a meta-analysis. Chin J Microecol 28:1257–1268
Woting A, Blaut M (2016) The intestinal microbiota in metabolic disease. Nutrients 8:1–19. https://doi.org/10.3390/nu8040202
Kobyliak N, Tetyana F, Oleksandr V et al (2016) Comparative experimental investigation on the efficacy of mono- and multiprobiotic strains in non-alcoholic fatty liver disease prevention. BMC Gastroenterol 16(34):1–9. https://doi.org/10.1186/s12876-016-0451-2
Ryan PM, Ross RP, Fitzgerald GF et al (2015) Functional food addressing heart health: do we have to target the gut microbiota? Curr Opin Clin Nutr Metab Care 18(6):566–571. https://doi.org/10.1097/MCO.0000000000000224
Moss JW, Ramji DP et al (2016) Nutraceutical therapies for atherosclerosis. Nat Rev Cardiol 13:513–532. https://doi.org/10.1038/nrcardio.2016.103
Madjd TMA, Mousavi N et al (2016) Comparison of the effect of daily consumption of probiotic compared with low-fat conventional yogurt on weight loss in healthy obese women following an energy-restricted diet: a randomized controlled trial. Am J Clin Nutr 103:323–329. https://doi.org/10.3945/ajcn.115.120170
Michael DR, Moss JW, Calvente DL et al (2016) Lactobacillus plantarum CUL66 can impact cholesterol homeostasis in Caco-2 enterocytes. Benef Microbes 7(3):443–451. https://doi.org/10.3920/BM2015.0146
Shehataet MG, El Sohaimy SA, Malak A et al (2016) Screening of isolated potential probiotic lactic acid bacteria for cholesterol lowering property and bile salt hydrolase activity. Ann Agric Sci 61:65–75. https://doi.org/10.1016/j.aoas.2016.03.001
Sieo SM, Sieo CC, Ramasamy K et al (2014) Effects of dietary prebiotics, probiotic and synbiotics on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens. J Sci Food Agric 94:341–348. https://doi.org/10.1002/jsfa.6365
Antikainen J, Korhonen TK, Kuparinen V (2009) Surface proteins of Lactobacillus involved in host interactions. In: Ljungh A, Wadström T (eds) Lactobacillus molecular biology: from genomics to probiotics. Caister Academic Press, Norfolk, pp 95–114
Ait Seddik H, Bendali F, Cudennec B, Drider D (2017) Anti-pathogenic and Probiotic attributes of Lactobacillus salivarius and Lactobacillus plantarum strains isolated from feces of Algerian infants and adults. Res Microbiol 168(3):244–254
Mann GV, Spoerry A (1974) Studies of a surfactant and cholesteremia in the Maasai. Am J Clin Nutr 27:464–469
Bendali F, Kerdouche K, Hamma-Faradji S, Drider D (2017) In vitro and in vivo cholesterol lowering ability of Lactobacillus pentosus KF923750. Benef Microbes 8(2):271–280. https://doi.org/10.3920/BM2016.0121
Del Re B, Sgorbati B et al (2000) Auto-aggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31:438
Lambert JM, Bongers RS, de Vos WM et al (2008) Functional analysis of four bile salt hydrolase and penicillin acylase family members in Lactobacillus plantarum WCFS1. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00137-08
Elkins CA, Moser SA, Savage DC et al (2001) Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonii 100–100 and other Lactobacillus species. Microbiology 147:3403–3412. https://doi.org/10.1099/00221287-147-12-3403
Corzo G, Gilliland SE (1999) Bile salt hydrolase activity of three strains of Lactobacillus acidophilus. J Dairy Sci 82(3):472–480. https://doi.org/10.3168/jds.S0022-0302(99)75256-2
Tanaka H, Doesburg K, Iwasaki T et al (1999) Screening of lactic acid bacteria for bile salt hydrolase activity. J Dairy Sci 82(12):2530–2535. https://doi.org/10.3168/jds.S0022-0302(99)75506-2
Papadimitriou K, Zoumpopoulou G, Foligné B et al (2015) Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front Microbiol 6:58. https://doi.org/10.3389/fmicb.2015.00058
Gilliland SE, Nelson CR, Maxwell C (1985) Assimilation of cholesterol by Lactobacillus acidophilus. Appl Environ Microbiol 49(2):377–381
Taranto MP, Medici M, Perdigon G et al (1998) Evidence for hypocholesterolemic effect of Lactobacillus reuteri in hypercholesterolemicmice. J Dairy Sci 81(9):2336–2340. https://doi.org/10.3168/jds.S0022-0302(98)70123-7
Lin SY, Ayres JW, Winkler W Jr et al (1989) Lactobacillus effects on cholesterol: in vitro and in vivo results. J Dairy Sci 72(11):2885–2899. https://doi.org/10.3168/jds.S0022-0302(89)79439-X
Mohan JC, Arora R, Khalilullah M et al (1990) Preliminary observations on effect of Lactobacillus sporogenes on serum lipid levels in hypercholesterolemic patients. Indian J Med Res 92:431–432
Jones ML, Martoni CJ et al (2011) Cholesterol-lowering efficacy of a microencapsulated bile salt hydrolase-active Lactobacillus reuteri NCIMB 30242 yoghurt formulation in hypercholesterolaemic adults. Br J Nutr 9:1–9. https://doi.org/10.1006/pmed.1998.0401
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
Kumar S, Taylor WR, Thornton JM et al (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Acknowledgement
We take this opportunity to express our profound gratitude and deep regards to Jaypee Institute of Information Technology for their kind co-operation and encouragement.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Khare, A., Gaur, S. Cholesterol-Lowering Effects of Lactobacillus Species. Curr Microbiol 77, 638–644 (2020). https://doi.org/10.1007/s00284-020-01903-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-020-01903-w