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A Rapid and Specific Method for the Detection of Indole in Complex Biological Samples
Open accessAbstract
Indole, a bacterial product of tryptophan degradation, has a variety of important applications in the pharmaceutical industry and is a biomarker in biological and clinical specimens. Yet, specific assays to quantitate indole are complex and require expensive equipment and a high level of training. Thus, indole in biological samples is often estimated using the simple and rapid Kovács assay, which nonspecifically detects a variety of commonly occurring indole analogs. We demonstrate here a sensitive, specific, and rapid method for measuring indole in complex biological samples using a specific reaction between unsubstituted indole and hydroxylamine. We compared the hydroxylamine-based indole assay (HIA) to the Kovács assay and confirmed that the two assays are capable of detecting microgram amounts of indole. However, the HIA is specific to indole and does not detect other naturally occurring indole analogs. We further demonstrated the utility of the HIA in measuring indole levels in clinically relevant biological materials, such as fecal samples and bacterial cultures. Mean and median fecal indole concentrations from 53 healthy adults were 2.59 mM and 2.73 mM, respectively, but varied widely (0.30 mM to 6.64 mM) among individuals. We also determined that enterotoxigenic Escherichia coli strain H10407 produces 3.3 ± 0.22 mM indole during a 24-h period in the presence of 5 mM tryptophan. The sensitive and specific HIA should be of value in a variety of settings, such as the evaluation of various clinical samples and the study of indole-producing bacterial species in the gut microbiota.
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“In human feces, indole is detectable at micromolar concentrations (Darkoh et al., 2015)”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Darkoh et al., 2015
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“The Kovács method is the most commonly used to detect the indole concentration in various biological samples (50).”
MethodSinha, A. K., Laursen, M. F., Brinck, J. E., Rybtke, M., Hjørne, A. P., Procházková, N., Pedersen, M., Roager, H. M., & Licht, T. R. (2024) · Nature Microbiology · doi:10.1038/s41564-024-01737-3 · Cited by 313
“Notably, indole is the most abundant tryptophan metabolite detected in mouse caecal contents as well as in human faeces 21,22 .”
Intestinal microbiota-derived tryptophan metabolites are predictive of Ah receptor activity
Dong, F., Hao, F., Murray, I. A., Smith, P. B. W., Koo, I., Tindall, A. M., Kris‐Etherton, P. M., Gowda, K., Amin, S., Patterson, A. D., et al. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1788899 · Cited by 252
“Consistent with previous reports, it is clear that indole, in both mouse cecal contents and human stool, represents the most abundant of the tryptophan metabolites examined.(54) Another key feature of this study is the prominent species-dependent activity of these microbial tryptophan metabolites with regard to either…”
ResultNew Insights Into Gut-Bacteria-Derived Indole and Its Derivatives in Intestinal and Liver Diseases
Li, X., Zhang, B., Hu, Y., & Zhao, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.769501 · Cited by 244
“64 millimole in healthy adults), which indicates that there are very large individual differences in indole metabolism (Darkoh et al., 2015).”
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Hou, Y., Li, J., & Ying, S. (2023) · Metabolites · doi:10.3390/metabo13111166 · Cited by 244
Methods of detection of food-borne pathogens: a review
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Gut Bacteria and Hydrogen Sulfide: The New Old Players in Circulatory System Homeostasis
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“Indole was detected in mammalian feces [150–152], and gut bacteria produce indole presumably by enzymes homologous to tryptophanases [33].”
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Impact of Microbial Metabolites on Microbiota–Gut–Brain Axis in Inflammatory Bowel Disease
Banfi, D., Moro, E., Bosi, A., Bistoletti, M., Cerantola, S., Crema, F., Maggi, F., Giron, M. C., Giaroni, C., & Baj, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041623 · Cited by 160
“Despite of the limited number of reliable methods for the determination of microbial TRP catabolites in human biological specimens, available data suggest that the indole, IAA, and IPA are the most abundant microbial TRP catabolites in the human body [313,314].”
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Diverse roles of microbial indole compounds in eukaryotic systems
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“3 to 6 mM) have been detected in the fecal samples of healthy individuals indicating the abundance of indoleproducing bacteria in the gut (Darkoh et al., 2015; Hubbard, Murray & Perdew, 2015b; Chappell et al., 2016; Dong et al., 2020; Dvo r ak et al., 2020).”
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Zarkan, A., Liu, J., Matuszewska, M., Gaimster, H., & Summers, D. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2020.02.007 · Cited by 104
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Biosynthesis of the Enterotoxic Pyrrolobenzodiazepine Natural Product Tilivalline
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“(26), concomitant production of both cytotoxins TV and TM in the gut is expected.”
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“Indole concentration was determined in triplicates using the hydroxylamine indole assay (15).”
MethodInfluentialSelf-citationLiu, Y., Pei, Z., Pan, T., Wang, H., Chen, W., & Lu, W. (2023) · Microbiological Research · doi:10.1016/j.micres.2023.127392 · Cited by 88
Fecal Indole as a Biomarker of Susceptibility to Cryptosporidium Infection
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“Previously, healthy subjects showed a wide distribution of FICs, with 75% in the 1 to 4 mM range (15), and 80% of the baseline indole levels in a subset of 50 subjects used in the present study were in the same range.”
BackgroundMethodSelf-citationMicrobial Tryptophan Metabolism Tunes Host Immunity, Metabolism, and Extraintestinal Disorders
Liu, M., Nieuwdorp, M., de Vos, W. M., & Rampanelli, E. (2022) · Metabolites · doi:10.3390/metabo12090834 · Cited by 86
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Biphasic chemotaxis of Escherichia coli to the microbiota metabolite indole
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Shaw, C. A., Hess, M., & Weimer, B. C. (2023) · Microorganisms · doi:10.3390/microorganisms11071825 · Cited by 73
“Indole concentrations in feces of healthy individuals range widely, and studies suggest there are many factors contributing to this variance, including microbiome diversity, free exogenous Trp, and the availability of other substrates [103,111].”
BackgroundMicrobial Metabolite Regulation of Epithelial Cell-Cell Interactions and Barrier Function
Ornelas, A., Dowdell, A. S., Lee, J. S., & Colgan, S. P. (2022) · Cells · doi:10.3390/cells11060944 · Cited by 69
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Xing, P. Y., Pettersson, S., & Kundu, P. (2020) · PROTEOMICS · doi:10.1002/pmic.201800419 · Cited by 55
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“Many common gut bacteria are capable of producing indoles and the fecal indole concentration ranges between 1 and 4 mM.(120,121) Common indole metabolites include indole-3-pyruvate, indole-3-acetaldehyde, indole-3-lactic acid, indole-3-acetic acid, indole-3-acetamide, and indole-3-propionic acid.”
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Indole Pulse Signalling Regulates the Cytoplasmic pH of E. coli in a Memory-Like Manner
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Production of indigo through the use of a dual-function substrate and a bifunctional fusion enzyme
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“In our previous study, expression of PTDH-FMO resulted in about 60 mg of purified fusion enzyme per liter of culture [28].”
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“However, Kovac’s reagent tends to react with all indole containing compounds and this nonspecific reaction limits the application of Kovac’s assay for quantitative detection.(26) On the other hand, chromatographic techniques such as high-performance liquid chromatography and gas chromatography–mass spectrometry (GC–MS…”
MethodSynbiotics Alleviate the Gut Indole Load and Dysbiosis in Chronic Kidney Disease
Yang, C., Chen, T.-W., Lu, W.-L., Liang, S., Huang, H., Tseng, C., & Tarng, D. (2021) · Cells · doi:10.3390/cells10010114 · Cited by 49
“The Kovács analysis was based on a previous publication [32] and modified using 100 μL of the above-described indole standards in 70% ethanol or samples of unknown”
MethodIndole signaling decreases biofilm formation and related virulence of Listeria monocytogenes
Rattanaphan, P., Mittraparp‐arthorn, P., Srinoun, K., Vuddhakul, V., & Tansila, N. (2020) · FEMS Microbiology Letters · doi:10.1093/femsle/fnaa116 · Cited by 47
Lu, S., Wang, C., Ma, J., & Wang, Y. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1456030 · Cited by 49
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“According to previous reports [25,30,40], urinary indican and skatole were considered normal at values lower than 10 mg/L and 10 μg/L, respectively.”
ResultBacterial Indole as a Multifunctional Regulator of Klebsiella oxytoca Complex Enterotoxicity
Ledala, N., Malik, M., Rezaul, K., Paveglio, S. A., Provatas, A. A., Kiel, A., Caimano, M. J., Zhou, Y., Lindgren, J., Krasulová, K., et al. (2022) · mBio · doi:10.1128/mbio.03752-21 · Cited by 39
“The levels of indole in the intestinal lumen are unknown; however, concentrations in human feces can reach 6 mM (14), with most studies describing ranges between 0.”
BackgroundIndoles and the advances in their biotechnological production for industrial applications
Ferrer, L., Mindt, M., Wendisch, V., & Cankar, K. (2023) · Systems Microbiology and Biomanufacturing · doi:10.1007/s43393-023-00223-x · Cited by 31
“Another aspect in which indole signalling is relevant is on biological wastewater treatment plant since there is a significant concentration of indole in coal wastewater and in faeces from healthy adults ranging from 10 mg/L to 18.6 mg/L and 35.14 mg/L to 773.18 mg/L, respectively [39, 40].”
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Antibiofilm and Antimicrobial Activities of Chloroindoles Against Uropathogenic Escherichia coli
Boya, B. R., Lee, J., & Lee, J. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.872943 · Cited by 35
“Indole Assay Indole concentrations were determined using Kovac’s reagent as previously described (Darkoh et al., 2015).”
MethodHallmarks of the human intestinal microbiome on liver maturation and function
Almeida, J. I., Tenreiro, M. F., Martínez‐Santamaría, L., Guerrero‐Aspizua, S., Gisbert, J. P., Alves, P. M., Serra, M., & Baptista, P. M. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.10.015 · Cited by 37
Indole Inhibits ToxR Regulon Expression in Vibrio cholerae
Howard, M. F., Bina, X. R., & Bina, J. E. (2019) · Infection and Immunity · doi:10.1128/iai.00776-18 · Cited by 34
“hydroxylamine-based indole assay, as previously described (65).”
Antibacterial and Antibiofilm Activities of Chloroindoles Against Vibrio parahaemolyticus
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“This concentration of indole is representative of the highest concentration found in feces (Darkoh et al. 2015), thus presumably in the most distal part of the large intestine.”
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“All compounds were tested at concentrations of up to 200 μM, except for IAC (the maximum concentration was 100 μM due to solubility limitations) and IND (1 mM given its known high intestinal concentrations) [29,30].”
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“18 mg/L in feces from healthy adults (Carin et al., 2015; Darkoh et al. 2015; Wu et al. 2017; Zhu et al. 2017; Zhu et al. 2018).”
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Optical probe for the analysis of trace indole in shrimp
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“In addition, biochemical tests are coupled with culture-based methods to confirm the biological and chemical characteristics of specific foodborne pathogens [5].”
Biotherapeutic potential of gut microbiota-derived indole-3-acetic acid
Yang, J., Wang, H., Yan, J., Sun, J., Wang, Y., Huang, G., Zhang, F., Cao, H., & Li, D. (2025) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2025.2532611 · Cited by 14
“Fecal indole concentrations span 0.25–4.0 mM (Darkoh et al. 2015; chappell et al. 2016; ledala et al. 2022), whereas iAA exhibits compartment-specific distribution with 5 μM in feces and 119.6 μM in systemic circulation (vyhlídalová et al. 2020; Fabresse et al. 2023).”
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“However, a high level of indole can still accumulate at enteric sites [36].”
BackgroundThe Other Obesity Epidemic—Of Drugs and Bugs
Sfera, A., Osorio, C. P., Diaz, E. L., Maguire, G., & Cummings, M. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00488 · Cited by 13
Indole at low concentration helps exponentially growing Escherichia coli survive at high temperature
Liu, J., & Summers, D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188853 · Cited by 12
Microbial Indoles: Key Regulators of Organ Growth and Metabolic Function
Xing, P. Y., Agrawal, R., Jayaraman, A., Martin, K. A., Zhang, G. W., Ngu, E.-L., Faylon, L. E., Kjelleberg, S. J., Rice, S. A., Wang, Y., et al. (2024) · Microorganisms · doi:10.3390/microorganisms12040719 · Cited by 10
“In contrast, indole concentrations in healthy mice and humans have been reported to be about 80 nmol/g and 145 nmol/g of fecal samples, respectively [5,6].”
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“Hydroxylamine-Based Indole Assay (HIA) HIA was performed according to a previous paper describing the determination of indole concentration (21).”
MethodMicrobial tryptophan catabolism as an actionable target via diet-microbiome interactions
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Indole-mediated reconfiguration of soil microbial consortia in response to microplastic pollution
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“Indole is the most abundant L-TRP metabolite of the normal human fecal metabolome (~ 3mM) [3, 135] and its levels correlate with those of serum indoxyl sulfate [115].”
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“Additionally, the indole assay provides a quantitative method for detecting indole levels (47).”
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Self-citationpH regulates gut bacterial tryptophan metabolism
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Biosynthese des enterotoxischen Pyrrolobenzodiazepin‐Naturstoffs Tilivallin
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Metadata
- Authors
- Darkoh, C., Chappell, C., Gonzales, C., & Okhuysen, P.
- Affiliations
- The University of Texas Health Science Center at Houston (US)
- The University of Texas MD Anderson Cancer Center (US)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2015-12
- Volume
- 81
- Issue
- 23
- Pages
- 8093-8097
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC4651089
- OpenAlex
- W2260701616
- Semantic Scholar
- c738683cc725688e7523668357b4d9797097bcfa
- Cited by
- 156
- References
- 31
- Citations by year
- 2026: 21 · 2025: 19 · 2024: 13 · 2023: 27 · 2022: 18 · 2021: 12 · 2020: 17 · 2019: 12 · 2018: 10 · 2017: 4 · 2016: 2
- FWCI
- 4.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (R01AI116914)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK56338, P30DK056338)
- Topics
- Health Sciences › Medicine › Microbiology (medical) › Bacterial Identification and Susceptibility Testing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Polyamine Metabolism and Applications
- Physical Sciences › Chemistry › Analytical Chemistry › Analytical Methods in Pharmaceuticals
- Keywords
- tryptophan degradation, enterotoxigenic Escherichia coli, gut microbiota, biomarkers, bacterial metabolites
- MeSH terms
- Bacteriological Techniques, Environmental Microbiology, Feces, Humans, Indoles, Sensitivity and Specificity, Tryptophan, Hydroxylamine, Enterotoxigenic Escherichia coli
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