Production of Indole-3-Lactic Acid by Bifidobacterium Strains Isolated fromHuman Infants

Takuma Sakurai; Toshitaka Odamaki; Jin-Zhong Xiao

doi:10.3390/microorganisms7090340

journal article Open Access Sep 11, 2019

Production of Indole-3-Lactic Acid by Bifidobacterium Strains Isolated fromHuman Infants

Takuma Sakurai Toshitaka Odamaki

Jin-Zhong Xiao

Microorganisms Vol. 7 No. 9 pp. 340 · MDPI AG

View at Publisher Save 10.3390/microorganisms7090340

Abstract

Recent studies have shown that metabolites produced by microbes can be considered as mediators of host-microbial interactions. In this study, we examined the production of tryptophan metabolites by Bifidobacterium strains found in the gastrointestinal tracts of humans and other animals. Indole-3-lactic acid (ILA) was the only tryptophan metabolite produced in bifidobacteria culture supernatants. No others, including indole-3-propionic acid, indole-3-acetic acid, and indole-3-aldehyde, were produced. Strains of bifidobacterial species commonly isolated from the intestines of human infants, such as Bifidobacterium longum subsp. longum, Bifidobacterium longum subsp. infantis, Bifidobacterium breve, and Bifidobacterium bifidum, produced higher levels of ILA than did strains of other species. These results imply that infant-type bifidobacteria might play a specific role in host–microbial cross-talk by producing ILA in human infants.

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References

34

[1]

Impact of the Gut Microbiota on Intestinal Immunity Mediated by Tryptophan Metabolism

Jing Gao, Kang Xu, Hongnan Liu et al.

Frontiers in Cellular and Infection Microbiology 2018 10.3389/fcimb.2018.00013

[2]

Roager "Microbial tryptophan catabolites in health and disease" Nat. Commun. (2018) 10.1038/s41467-018-05470-4

[3]

Krishnan "Gut microbiota-derived tryptophan metabolites modulate inflammatory response in hepatocytes and macrophages" Cell Rep. (2018) 10.1016/j.celrep.2018.03.109

[4]

Hou "Lactobacillus accelerates ISCS regeneration to protect the integrity of intestinal mucosa through activation of stat3 signaling pathway induced by LPLs secretion of IL-22" Cell Death Differ. (2018) 10.1038/s41418-018-0070-2

[5]

Venkatesh "Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4" Immunity (2014) 10.1016/j.immuni.2014.06.014

[6]

Morshedi "Inhibition of amyloid fibrillation of lysozyme by indole derivatives--possible mechanism of action" FEBS J. (2007) 10.1111/j.1742-4658.2007.06158.x

[7]

Ichida "Prevention of UVB-induced production of the inflammatory mediator in human keratinocytes by lactic acid derivatives generated from aromatic amino acids" Biosci. Biotechnol. Biochem. (2013) 10.1271/bbb.120979

[8]

Suzuki "Identification of antioxidants produced by Lactobacillus plantarum" Biosci. Biotechnol. Biochem. (2013) 10.1271/bbb.121006

[9]

Lactobacillus reuteri induces gut intraepithelial CD4 + CD8αα + T cells

Luisa Cervantes-Barragan, Jiani N. Chai, Ma. Diarey Tianero et al.

Science 2017 10.1126/science.aah5825

[10]

Salt-responsive gut commensal modulates TH17 axis and disease

Nicola Wilck, Mariana G. Matus, Sean M. Kearney et al.

Nature 2017 10.1038/nature24628

[11]

Peters, A., Krumbholz, P., Jager, E., Heintz-Buschart, A., Cakir, M.V., Rothemund, S., Gaudl, A., Ceglarek, U., Schoneberg, T., and Staubert, C. (2019). Metabolites of lactic acid bacteria present in fermented foods are highly potent agonists of human hydroxycarboxylic acid receptor 3. PLoS Genet., 15. 10.1371/journal.pgen.1008283

[12]

Aragozzini "Indole-3-lactic acid as a tryptophan metabolite produced by Bifidobacterium spp." Appl. Environ. Microbiol. (1979) 10.1128/aem.38.3.544-546.1979

[13]

Smith "Enumeration of human colonic bacteria producing phenolic and indolic compounds: Effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism" J. Appl. Bacteriol. (1996) 10.1111/j.1365-2672.1996.tb04331.x

[14]

Turroni, F., Peano, C., Pass, D.A., Foroni, E., Severgnini, M., Claesson, M.J., Kerr, C., Hourihane, J., Murray, D., and Fuligni, F. (2012). Diversity of bifidobacteria within the infant gut microbiota. PLoS ONE, 7. 10.1371/journal.pone.0036957

[15]

Ishikawa "Ethnic diversity of gut microbiota: Species characterization of Bacteroides fragilis group and genus Bifidobacterium in healthy Belgian adults, and comparison with data from Japanese subjects" J. Biosci. Bioeng. (2013) 10.1016/j.jbiosc.2013.02.010

[16]

Odamaki "Comparative genomics revealed genetic diversity and species/strain-level differences in carbohydrate metabolism of three probiotic bifidobacterial species" Int. J. Genom. (2015)

[17]

"Bifidobacteria and their role as members of the human gut microbiota" Front. Microbiol. (2016)

[18]

Duranti "Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum" Environ. Microbiol. (2015) 10.1111/1462-2920.12743

[19]

Kato "Age-related changes in the composition of gut Bifidobacterium species" Curr. Microbiol. (2017) 10.1007/s00284-017-1272-4

[20]

Odamaki "Impact of a bathing tradition on shared gut microbe among Japanese families" Sci. Rep. (2019) 10.1038/s41598-019-40938-3

[21]

Lin "A review of the relationship between the gut microbiota and amino acid metabolism" Amino Acids (2017) 10.1007/s00726-017-2493-3

[22]

Liu, Y., Alookaran, J.J., and Rhoads, J.M. (2018). Probiotics in autoimmune and inflammatory disorders. Nutrients, 10. 10.20944/preprints201809.0397.v1

[23]

Mashiguchi "The main auxin biosynthesis pathway in Arabidopsis" Proc. Natl. Acad. Sci. USA (2011) 10.1073/pnas.1108434108

[24]

Gilbert "Bacterial production of indole related compounds reveals their role in association between duckweeds and endophytes" Front. Chem. (2018) 10.3389/fchem.2018.00265

[25]

Wong "Different physiological properties of human-residential and non-human-residential bifidobacteria in human health" Benef. Microbes (2018) 10.3920/bm2017.0031

[26]

Morita "Bifidobacterium kashiwanohense sp. Nov., isolated from healthy infant faeces" Int. J. Syst. Evol. Microbiol. (2011) 10.1099/ijs.0.024521-0

[27]

Nishizawa "Molecular analysis of the rebeccamycin L-amino acid oxidase from Lechevalieria aerocolonigenes ATCC 39243" J. Bacteriol. (2005) 10.1128/jb.187.6.2084-2092.2005

[28]

A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites

DYLAN DODD, Matthew H. Spitzer, William Van Treuren et al.

Nature 2017 10.1038/nature24661

[29]

Matteoli "Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction" Gut (2010) 10.1136/gut.2009.185108

[30]

Lanz "Suppression of Th1 differentiation by tryptophan supplementation in vivo" Amino Acids (2017) 10.1007/s00726-017-2415-4

[31]

Age-Associated Microbial Dysbiosis Promotes Intestinal Permeability, Systemic Inflammation, and Macrophage Dysfunction

Netusha Thevaranjan, Alicja Puchta, Christian Schulz et al.

Cell Host & Microbe 2017 10.1016/j.chom.2017.03.002

[32]

Inflammaging: a new immune–metabolic viewpoint for age-related diseases

Claudio Franceschi, Paolo Garagnani, Paolo Parini et al.

Nature Reviews Endocrinology 2018 10.1038/s41574-018-0059-4

[33]

Shigeno "Gut microbiota development in mice is affected by hydrogen peroxide produced from amino acid metabolism during lactation" FASEB J. (2019) 10.1096/fj.201801462r

[34]

Dieuleveux "Antimicrobial spectrum and target site of D-3-phenyllactic acid" Int. J. Food Microbiol. (1998) 10.1016/s0168-1605(98)00031-2

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References

Details

Published: Sep 11, 2019
Vol/Issue: 7(9)
Pages: 340
License: View

Authors

T

Takuma Sakurai

Next Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama, Kanagawa 252-8583, Japan

T

Toshitaka Odamaki

Next Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama, Kanagawa 252-8583, Japan

J

Jin-Zhong Xiao

Next Generation Science Institute, Morinaga Milk Industry Co., Ltd., Zama, Kanagawa 252-8583, Japan

Cite This Article

Takuma Sakurai, Toshitaka Odamaki, Jin-Zhong Xiao (2019). Production of Indole-3-Lactic Acid by Bifidobacterium Strains Isolated fromHuman Infants. Microorganisms, 7(9), 340. https://doi.org/10.3390/microorganisms7090340

Production of Indole-3-Lactic Acid by Bifidobacterium Strains Isolated fromHuman Infants

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