Abstract
Indole is a typical heterocyclic compound derived from tryptophan widespread in nature. Pseudomonas aeruginosa is one of the most common opportunistic pathogens everywhere in the world. Indole and P. aeruginosa will encounter inevitably; however, the indole transformation process by P. aeruginosa remains unclear. Herein, an indole-degrading strain of P. aeruginosa Jade-X was isolated from activated sludge. Strain Jade-X could degrade 1 mmol/L indole within 48 h with the inoculum size of 1% (v/v). It showed high efficiency in indole degradation under the conditions of 30–42 °C, pH 5.0–9.0, and NaCl concentration less than 2.5%. The complete genome of strain Jade-X was sequenced which was 6508614 bp in length with one chromosome. Bioinformatic analyses showed that strain Jade-X did not contain the indole oxygenase gene. Three cytochrome P450 genes were identified and up-regulated in the indole degradation process by RT-qPCR analysis, while cytochrome P450 inhibitors did not affect the indole degradation process. It suggested that indole oxidation was catalyzed by an unraveled enzyme. An ant gene cluster was identified, among which the anthranilate 1,2-dioxygenase and catechol 1,2-dioxygenase genes were upregulated. An indole-anthranilate-catechol pathway was proposed in indole degradation by strain P. aeruginosa Jade-X. This study enriched our understanding of the indole biodegradation process in P. aeruginosa.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The genomic sequences of strain Jade-X were deposited in the GenBank with accession number CP114374.1. The datasets generated during the current study are available from the corresponding author upon reasonable request.
References
Coleman JP, Hudson LL, McKnight SL, Farrow JM III, Calfee MW, Lindsey CA, Pesci EC (2008) Pseudomonas aeruginosa PqsA is an anthranilate-coenzyme A ligase. J. Bacteriol 190(4):1247–1255
Doukyu N, Aono R (1997) Biodegradation of indole at high concentration by persolvent fermentation with Pseudomonas sp. ST-200. Extremophiles 1:100–105
Ensley BD, Ratzkin BJ, Osslund TD et al (1983) Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 222(4620):167–169
Fabara AN, Fraaije MW (2020) An overview of microbial indigo-forming enzymes. Appl Microbiol Biotechnol 104(3):925–933
Farrow JM III, Pesci EC (2007) Two distinct pathways supply anthranilate as a precursor of the Pseudomonas quinolone signal. J Bacteriol 189(9):3425–3433
Garbe TR, Kobayashi M, Yukawa H (2000) Indole-inducible proteins in bacteria suggest membrane and oxidant toxicity. Arch Microbiol 173:78–82
Heine T, Großmann C, Hofmann S et al (2019) Indigoid dyes by group E monooxygenases: mechanism and biocatalysis. Biol Chem 400(7):939–950
Hwang HJ, Li XH, Kim SK et al (2022) Anthranilate acts as a signal to modulate biofilm formation, virulence, and antibiotic tolerance of Pseudomonas aeruginosa and surrounding bacteria. Microbiol. Spectr 10(1):e01463–e01421
Lee JH, Wood TK, Lee J (2015) Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23:707–718
Lee J, Attila C, Cirillo SLG et al (2009) Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2(1):75–90
Li S, Du L, Bernhardt R (2020) Redox partners: function modulators of bacterial P450 enzymes. Trends Microbiol 28(6):445–454
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Kim J, Hong H, Heo A et al (2013) Indole toxicity involves the inhibition of adenosine triphosphate production and protein folding in Pseudomonas putida. FEMS Microbiol Lett 343:89–99
Kim M, Lee JH, Kim E et al (2016) Isolation of indole utilizing bacteria Arthrobacter sp. and Alcaligenes sp. from livestock waste. Indian J Microbiol 56:158–166
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547
Ma Q, Zhang X, Qu Y (2018) Biodegradation and biotransformation of indole: advances and perspectives. Front Microbiol 9:2625
Ma Q, Liu Z, Yang B et al (2019) Characterization and functional gene analysis of a newly isolated indole-degrading bacterium Burkholderia sp. IDO3. J Hazard Mater 367:144–151
Ma Q, Meng N, Su J et al (2023) Unraveling the skatole biodegradation process in an enrichment consortium using integrated omics and culture-dependent strategies. J Environ Sci 127:688–699
Palmer GC, Jorth PA, Whiteley M (2013) The role of two Pseudomonas aeruginosa anthranilate synthases in tryptophan and quorum signal production. Microbiology 159:959–969
Pang Z, Raudonis R, Glick BR et al (2019) Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv 37(1):177–192
Qu Y, Ma Q, Liu Z et al (2017) Unveiling the biotransformation mechanism of indole in a Cupriavidus sp. strain. Mol Microbiol 106:905–918
Sadauskas M, Vaitekunas J, Gasparaviciute R et al (2017) Indole biodegradation in Acinetobacter sp. strain O153: genetic and biochemical characterization. Appl Environ Microbiol 83(19):e01453–e01417
Stover CK, Pham XQ, Erwin AL et al (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406(6799):959–964
Wei K, Yin H, Peng H et al (2018) Bioremediation of triphenyl phosphate by Brevibacillus brevis: degradation characteristics and role of cytochrome P450 monooxygenase. Sci Total Environ 627:1389–1395
Yin B, Gu JD, Wan N (2005) Degradation of indole by enrichment culture and Pseudomonas aeruginosa Gs isolated from mangrove sediment. Int Biodeterior Biodegradation 56(4):243–248
Zarkan A, Liu J, Matuszewska M et al (2020) Local and universal action: the paradoxes of indole signalling in bacteria. Trends Microbiol 28(7):566–577
Zhang X, Jing J, Zhang L et al (2019) Biodegradation characteristics and genomic functional analysis of indole-degrading bacterial strain Acinetobacter sp. JW. J Chem Technol Biotechnol 94(4):1114–1122
Funding
The study was supported by the National Natural Science Foundation of China (No. 32170121).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by QM, JZ, CW, and SL. The first draft of the manuscript was written by JZ, QM, and SF. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Consent for publication
All authors have approved the manuscript and agree with its publication.
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, J., Ma, Q., Wang, C. et al. Biodegradation characteristics and genomic analysis of a newly isolated indole-degrading strain Pseudomonas aeruginosa Jade-X. Int Microbiol 27, 449–457 (2024). https://doi.org/10.1007/s10123-023-00408-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-023-00408-3