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Differential expression of urease genes and ureolytic activity of uropathogenic Escherichia coli and Pseudomonas aeruginosa isolates in different nutritional conditions.

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Title: Differential expression of urease genes and ureolytic activity of uropathogenic Escherichia coli and Pseudomonas aeruginosa isolates in different nutritional conditions.
Authors: Subramaniyan Y; Division of Microbiology and Biotechnology, Yenepoya Research Centre, Yenepoya (Deemed to Be University), University Road, Deralakatte, Mangalore, 575018, India., Khan A; Department of Urology, Yenepoya Medical College and Hospital, Yenepoya (Deemed to Be University), University Road, Deralakatte, Mangalore, 575018, India., Fathima F; Division of Microbiology and Biotechnology, Yenepoya Research Centre, Yenepoya (Deemed to Be University), University Road, Deralakatte, Mangalore, 575018, India., Rekha PD; Division of Microbiology and Biotechnology, Yenepoya Research Centre, Yenepoya (Deemed to Be University), University Road, Deralakatte, Mangalore, 575018, India. rekhapd@yenepoya.edu.in.
Source: Archives of microbiology [Arch Microbiol] 2023 Nov 16; Vol. 205 (12), pp. 383. Date of Electronic Publication: 2023 Nov 16.
Publication Type: Journal Article
Language: English
Journal Info: Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0410427 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-072X (Electronic) Linking ISSN: 03028933 NLM ISO Abbreviation: Arch Microbiol Subsets: MEDLINE
Imprint Name(s): Original Publication: Berlin, New York, Springer-Verlag.
MeSH Terms: Pseudomonas aeruginosa*/genetics , Pseudomonas aeruginosa*/metabolism , Uropathogenic Escherichia coli*/genetics , Uropathogenic Escherichia coli*/metabolism, Urease/genetics ; Urease/metabolism ; Struvite ; Urea
Abstract: Uropathogens have adaptation strategies to survive in the host urinary tract by efficiently utilizing and tolerating the urinary metabolites. Many uropathogens harbour the enzyme urease for the breakdown of urea and the enzymatic breakdown of urea increases the pH and facilitate the struvite crystallization. In this study, the differential urease activity of uropathogenic Escherichia coli and Pseudomonas aeruginosa strains was investigated under different nutritional conditions. The experiments included measurement of growth, pH, urease activity, NH4-N generation and urease gene (ureC) expression among the bacterial strains under different conditions. Further, the implications of urea breakdown on the struvite crystallization in vitro and biofilm formation were also assessed. The study included urease positive isolates and for comparison urease negative isolates were included. Compared to the urease negative strains the urease positive strains formed higher biofilms and motility. The urease positive P. aeruginosa showed significantly higher (p < 0.01) pH and urease activity (A557-A630) compared to E. coli under experimental conditions. Further, supplementation of glucose to the growth media significantly increased the urease activity in P. aeruginosa and in contrast, it was significantly lower in E. coli. The expression profile of urease gene (ureC) was significantly higher (p < 0.001) in P. aeruginosa compared to E. coli and was consistent with the biochemical results of the urease activity under the nutritional conditions. The differential urease activity under two nutritional conditions influenced the biogenic struvite crystallization. It correlated with the urease activity showing higher crystallization rate in P. aeruginosa compared to E. coli. The results highlight the differential urease activity in two common uropathogens under different nutritional conditions that may have significant role on the regulation of virulence, pathogenicity and in the kidney stone disease.
(© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)
References: Alteri CJ, Mobley HL (2015) Metabolism and fitness of urinary tract pathogens. Metab Bact Pathog. https://doi.org/10.1128/9781555818883.ch10. (PMID: 10.1128/9781555818883.ch10)
Alteri CJ, Himpsl SD, Shea AE, Mobley HL (2019) Flexible metabolism and suppression of latent enzymes are important for Escherichia coli adaptation to diverse environments within the host. J Bacteriol 201:10–128. https://doi.org/10.1128/jb.00181-19. (PMID: 10.1128/jb.00181-19)
Arioli S, Della Scala G, Martinović A, Scaglioni L, Mazzini S, Volonté F, Pedersen MB, Mora D (2022) In Streptococcus thermophilus, ammonia from urea hydrolysis paradoxically boosts acidification and reveals a new regulatory mechanism of glycolysis. Microbiol Spectr 10(3):e02760–e02821. https://doi.org/10.1128/spectrum.02760-21. (PMID: 10.1128/spectrum.02760-21354674109241937)
Armbruster CE, Hodges SA, Mobley HL (2013) Initiation of swarming motility by Proteus mirabilis occurs in response to specific cues present in urine and requires excess L-glutamine. J Bacteriol 195:1305–1319. https://doi.org/10.1128/JB.02136-12. (PMID: 10.1128/JB.02136-12233160403591990)
Baethgen WE, Alley MM (1989) A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant Kjeldahl digests. Commun Soil Sci Plant Anal 20:961–969. https://doi.org/10.1080/00103628909368129. (PMID: 10.1080/00103628909368129)
Bayuseno AP, Perwitasari DS, Muryanto S, Tauviqirrahman M, Jamari J (2020) Kinetics and morphological characteristics of struvite (MgNH4PO4.6H2O) under the influence of maleic acid. Heliyon 6(3):e03533. https://doi.org/10.1016/j.heliyon.2020.e03533. (PMID: 10.1016/j.heliyon.2020.e03533322153257090354)
Burne RA, Chen YY (2000) Bacterial ureases in infectious diseases. Microbes Infect 2:533–542. https://doi.org/10.1016/s1286-4579(00)00312-9. (PMID: 10.1016/s1286-4579(00)00312-910865198)
Bury-Moné S, Skouloubris S, Labigne A, De Reuse H (2001) The Helicobacter pylori UreIprotein: role in adaptation to acidity and identification of residues essential for its activity and for acid activation. Mol Microbiol 42:1021–1034. https://doi.org/10.1046/j.1365-2958.2001.02689.x. (PMID: 10.1046/j.1365-2958.2001.02689.x11737644)
Carlini CR, Ligabue-Braun R (2016) Ureases as multifunctional toxic proteins: a review. Toxicon 110:90–109. https://doi.org/10.1016/j.toxicon.2015.11.020. (PMID: 10.1016/j.toxicon.2015.11.02026690979)
Chan CC, Lewis IA (2022) Role of metabolism in uropathogenic Escherichia coli. Trends Microbiol 30:1174–1204. https://doi.org/10.1016/j.tim.2022.06.003. (PMID: 10.1016/j.tim.2022.06.00335941063)
Chen YY, Burne RA (1996) Analysis of Streptococcus salivarius urease expression using continuous chemostat culture. FEMS Microbiol Lett 135:223–229. https://doi.org/10.1111/j.1574-6968.1996.tb07993.x. (PMID: 10.1111/j.1574-6968.1996.tb07993.x8595861)
Cole SJ, Records AR, Orr MW, Linden SB, Lee VT (2014) Catheter-associated urinary tract infection by Pseudomonas aeruginosa is mediated by exopolysaccharide-independent biofilms. Infect Immun 82:2048–2058. https://doi.org/10.1128/iai.01652-14. (PMID: 10.1128/iai.01652-14245951423993445)
Colin R, Ni B, Laganenka L, Sourjik V (2021) Multiple functions of flagellar motility and chemotaxis in bacterial physiology. FEMS Microbiol Rev 45(6):fuab038. https://doi.org/10.1093/femsre/fuab038. (PMID: 10.1093/femsre/fuab038342276658632791)
Dattelbaum JD, Lockatell CV, Johnson DE, Mobley HL (2003) UreR, the transcriptional activator of the Proteus mirabilis urease gene cluster, is required for urease activity and virulence in experimental urinary tract infections. Infect Immun 71(2):1026–1030. https://doi.org/10.1128/IAI.71.2.1026-1030.2003. (PMID: 10.1128/IAI.71.2.1026-1030.200312540589145398)
de Sousa T, Hébraud M, Alves O, Costa E, Maltez L, Pereira JE, Martins Â, Igrejas G, Poeta P (2023) Study of antimicrobial resistance, biofilm formation, and motility of Pseudomonas aeruginosa derived from urine samples. Microorganisms 11(5):1345. https://doi.org/10.3390/microorganisms11051345. (PMID: 10.3390/microorganisms110513453731731910224020)
Duran Ramirez JM, Gomez J, Obernuefemann CL, Gualberto NC, Walker JN (2022) Semi-quantitative assay to measure urease activity by urinary catheter-associated uropathogens. Front Cell Infect Microbiol 12:292. https://doi.org/10.3389/fcimb.2022.859093. (PMID: 10.3389/fcimb.2022.859093)
Flannigan RK, Battison A, De S, Humphreys MR, Bader M, Lellig E, Monga M, Chew BH, Lange D (2018) Evaluating factors that dictate struvite stone composition: a multi-institutional clinical experience from the EDGE Research Consortium. Can Urol Assoc J 12:131. https://doi.org/10.5489/cuaj.4804. (PMID: 10.5489/cuaj.480429319486)
Forsyth VS, Armbruster CE, Smith SN, Pirani A, Springman AC, Walters MS, Nielubowicz GR, Himpsl SD, Snitkin ES, Mobley HL (2018) Rapid growth of uropathogenic Escherichia coli during human urinary tract infection. Mbio 9(2):e00186-e218. https://doi.org/10.1128/mbio.00186-18. (PMID: 10.1128/mbio.00186-18295110755844997)
Fusco A, Coretti L, Savio V, Buommino E, Lembo F, Donnarumma G (2017) Biofilm formation and immunomodulatory activity of Proteus mirabilis clinically isolated strains. Int J Mol Sci 18(2):414. https://doi.org/10.3390/ijms18020414. (PMID: 10.3390/ijms18020414282122805343948)
González-Morales C, Fernández B, Molina FJ, Naranjo-Fernández D, Matamoros-Veloza A, Camargo-Valero MA (2021) Influence of pH and temperature on struvite purity and recovery from anaerobic digestate. Sustainability 13:10730. https://doi.org/10.3390/su131910730. (PMID: 10.3390/su131910730)
Griffith DP, Musher DM, Itin C (1976) Urease. The primary cause of infection-induced urinary stones. Invest Urol 13:346–350. (PMID: 815197)
Hothersall J, Osgerby A, Godfrey RE, Overton TW, Busby SJ, Browning DF (2022) New vectors for urea-inducible recombinant protein production. N Biotechnol 72:89–96. https://doi.org/10.1016/j.nbt.2022.10.003. (PMID: 10.1016/j.nbt.2022.10.00336273806)
Islam MJ, Bagale K, John PP, Kurtz Z, Kulkarni R (2022) Glycosuria alters uropathogenic Escherichia coli global gene expression and virulence. Msphere 7(3):e00004-22. https://doi.org/10.1128/msphere.00004-22. (PMID: 10.1128/msphere.00004-22354773019241551)
Jalil MB, Al Atbee MY (2022) The prevalence of multiple drug resistance Escherichia coli and Klebsiella pneumoniae isolated from patients with urinary tract infections. J Clin Lab 36:e24619. https://doi.org/10.1002/jcla.24619. (PMID: 10.1002/jcla.24619)
Jin D, Zhao S, Zheng N, Bu D, Beckers Y, Denman SE, McSweeney CS, Wang J (2017) Differences in ureolytic bacterial composition between the rumen digesta and rumen wall based on ureC gene classification. Front Microbiol 8:385. https://doi.org/10.3389/fmicb.2017.00385. (PMID: 10.3389/fmicb.2017.00385283260795339240)
Konieczna I, Zarnowiec P, Kwinkowski M, Kolesinska B, Fraczyk J, Kaminski Z, Kaca W (2012) Bacterial urease and its role in long-lasting human diseases. Curr Protein Pept 13:789–806. https://doi.org/10.2174/138920312804871094. (PMID: 10.2174/138920312804871094)
Korchef A, Abouda S, Souid I (2023) Optimizing struvite crystallization at high stirring rates. Crystals 13(4):711. https://doi.org/10.3390/cryst13040711. (PMID: 10.3390/cryst13040711)
Lai HC, Chang SN, Lin HC, Hsu YL, Wei HM, Kuo CC, Hwang KP, Chiang HY (2021) Association between urine pH and common uropathogens in children with urinary tract infections. J Microbiol Immunol Infect 54(2):290–298. https://doi.org/10.1016/j.jmii.2019.08.002. (PMID: 10.1016/j.jmii.2019.08.00231604680)
Lane MC, Alteri CJ, Smith SN, Mobley HL (2007) Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci USA 104:16669–16674. https://doi.org/10.1073/pnas.0607898104. (PMID: 10.1073/pnas.0607898104179254492034267)
Li X, Lu N, Brady HR, Packman AI (2016) Biomineralization strongly modulates the formation of Proteus mirabilis and Pseudomonas aeruginosa dual-species biofilms. FEMS Microbiol Ecol 92:frw189. https://doi.org/10.1093/femsec/fiw189. (PMID: 10.1093/femsec/fiw189)
Lila AS, Rajab AA, Abdallah MH, Rizvi SM, Moin A, Khafagy ES, Tabrez S, Hegazy WA (2023) Biofilm lifestyle in recurrent urinary tract infections. Life 13:148. https://doi.org/10.3390/life13010148. (PMID: 10.3390/life13010148366761009865985)
Liu S, Yu Z, Zhong H, Zheng N, Huws S, Wang J, Zhao S (2023) Functional gene-guided enrichment plus in situ microsphere cultivation enables isolation of new crucial ureolytic bacteria from the rumen of cattle. Microbiome 11:1–8. https://doi.org/10.1186/s40168-023-01510-4. (PMID: 10.1186/s40168-023-01510-4)
Maier RJ, Benoit SL (2019) Role of nickel in microbial pathogenesis. Inorganics 7(7):80. https://doi.org/10.3390/inorganics7070080. (PMID: 10.3390/inorganics7070080)
Mann R, Mediati G, Duggin IG, Harry EJ, Bottomley AL (2017) Metabolic adaptations of uropathogenic E. coli in the urinary tract. Front Cell Infect Microbiol 7:241. https://doi.org/10.3389/fcimb.2017.00241. (PMID: 10.3389/fcimb.2017.00241286428455463501)
Manzoor MA, Singh B, Agrawal AK, Arun AB, Mujeeburahiman M, Rekha PD (2018) Morphological and micro-tomographic study on evolution of struvite in synthetic urine infected with bacteria and investigation of its pathological biomineralization. PLoS ONE 13:e0202306. https://doi.org/10.1371/journal.pone.0202306. (PMID: 10.1371/journal.pone.0202306301069926091953)
McGill SL, Yung Y, Hunt KA, Henson MA, Hanley L, Carlson RP (2021) Pseudomonas aeruginosa reverse diauxie is a multidimensional, optimized, resource utilization strategy. Sci Rep 11:1457. https://doi.org/10.1038/s41598-020-80522-8. (PMID: 10.1038/s41598-020-80522-8334468187809481)
Nair A, Sarma SJ (2021) The impact of carbon and nitrogen catabolite repression in microorganisms. Microbiol Res 251:126831. https://doi.org/10.1016/j.micres.2021.126831. (PMID: 10.1016/j.micres.2021.12683134325194)
Norsworthy AN, Pearson MM (2017) From catheter to kidney stone: the uropathogenic lifestyle of Proteus mirabilis. Trends Microbiol 25(4):304–315. https://doi.org/10.1016/j.tim.2016.11.015. (PMID: 10.1016/j.tim.2016.11.01528017513)
Odoki M, AlmustaphaAliero A, Tibyangye J, Nyabayo Maniga J, Wampande E, Drago Kato C, Agwu E, Bazira J (2019) Prevalence of bacterial urinary tract infections and associated factors among patients attending hospitals in Bushenyi district, Uganda. Int J Microbiol. https://doi.org/10.1155/2019/4246780. (PMID: 10.1155/2019/4246780309063236397969)
Orth D, Grif K, Dierich MP, Würzner R (2006) Prevalence, structure and expression of urease genes in Shiga toxin-producing Escherichia coli from humans and the environment. Int J Hyg Environ Health 209:513–520. https://doi.org/10.1016/j.ijheh.2006.06.003. (PMID: 10.1016/j.ijheh.2006.06.00316877040)
Pompilio A, Crocetta V, Savini V, Petrelli D, Di Nicola M, Bucco S, Amoroso L, Bonomini M, Di Bonaventura G (2018) Phylogenetic relationships, biofilm formation, motility, antibiotic resistance and extended virulence genotypes among Escherichia coli strains from women with community-onset primitive acute pyelonephritis. PLoS ONE 13(5):e0196260. https://doi.org/10.1371/journal.pone.0196260. (PMID: 10.1371/journal.pone.0196260297580335951556)
Reitzer L, Zimmern P (2019) Rapid growth and metabolism of uropathogenic Escherichia coli in relation to urine composition. Clin Microbiol Rev 33:10–128. https://doi.org/10.1128/cmr.00101-19. (PMID: 10.1128/cmr.00101-19)
Rekha PD, Hameed A, Manzoor MAP, Suryavanshi MV, Ghate SD, Arun AB, Rao SS, Athmika BSK, Mujeeburahiman M, Young CC (2020) First report of pathogenic bacterium Kalamiella piersonii isolated from urine of a kidney stone patient: Draft genome and evidence for role in struvite crystallization. Pathogens 9:711. https://doi.org/10.3390/pathogens9090711.y. (PMID: 10.3390/pathogens9090711.y328723967558591)
Ridha Abbas Al-Fahham H, Raoof Kareem K (2022) Molecular study of urease ureR gene of Proteus mirabilis isolated from urinary tract infections, Najaf, Iraq. Institut Razi Arch. https://doi.org/10.22092/ari.2022.357465.2042. (PMID: 10.22092/ari.2022.357465.2042)
Righetto RD, Anton L, Adaixo R, Jakob RP, Zivanov J, Mahi MA, Ringler P, Schwede T, Maier T, Stahlberg H (2022) High-resolution cryo-EM structure of urease from the pathogen Yersinia enterocolitica. Nat Commun 11(1):5101. https://doi.org/10.1038/s41467-020-18870-2. (PMID: 10.1038/s41467-020-18870-2)
Salari N, Karami MM, Bokaee S (2022) The prevalence of urinary tract infections in type 2 diabetic patients: a systematic review and meta-analysis. Eur J Med Res 27:20. https://doi.org/10.1186/s40001-022-00644-9. (PMID: 10.1186/s40001-022-00644-9351235658817604)
Scavone P, Iribarnegaray V, González MJ, Navarro N, Caneles-Huerta N, Jara-Wilde J, Härtel S, Zunino P (2023) Role of Proteus mirabilis flagella in biofilm formation. Rev Argent Microbiol 55(3):226–234. https://doi.org/10.1016/j.ram.2023.01.005. (PMID: 10.1016/j.ram.2023.01.00537076397)
Sharndama HC, Mba IE (2022) Helicobacter pylori: An up-to-date overview on the virulence and pathogenesis mechanisms. Braz J Microbiol. https://doi.org/10.1007/s42770-021-00675-0. (PMID: 10.1007/s42770-021-00675-0349889378731681)
She P, Wang Y, Liu Y, Tan F, Chen L, Luo Z, Wu Y (2019) Effects of exogenous glucose on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. Microbiologyopen 12:e933. https://doi.org/10.1002/mbo3.933. (PMID: 10.1002/mbo3.933)
Sigurdarson JJ, Svane S, Karring H (2020) Development of a M9-based Urea Medium (M9U) for sensitive and real-time monitoring of ureolytic activity of bacteria and cell-free urease. Microbiologyopen 9:e976. https://doi.org/10.1002/mbo3.976. (PMID: 10.1002/mbo3.976319439187066460)
Sonkoue Lambou JC, Noubom M, Djoumsie Gomseu BE, Takougoum Marbou WJ, Tamokou JD, Gatsing D (2022) Multidrug-resistant Escherichia coli causing urinary tract infections among controlled and uncontrolled type 2 diabetic patients at Laquintinie Hospital in Douala, Cameroon. Can J Infect Dis Med Microbiol. https://doi.org/10.1155/2022/1250264. (PMID: 10.1155/2022/1250264366247999825230)
Su J, Jin L, Jiang Q, Sun W, Zhang F, Li Z (2013) Phylogenetically diverse ureC genes and their expression suggest the urea utilization by bacterial symbionts in marine sponge Xestospongia testudinaria. PLoS ONE 8:e64848. https://doi.org/10.1371/journal.pone.0064848. (PMID: 10.1371/journal.pone.0064848237414043669342)
Vipin C, Mujeeburahiman M, Arun AB, Ashwini P, Mangesh SV, Rekha PD (2019) Adaptation and diversification in virulence factors among urinary catheter-associated Pseudomonas aeruginosa isolates. J Appl Microbiol 126(2):641–650. https://doi.org/10.1111/jam.14143. (PMID: 10.1111/jam.1414330372578)
Vipin C, Saptami K, Fida F, Mujeeburahiman M, Rao SS, Athmika AAB, Rekha PD (2020) Potential synergistic activity of quercetin with antibiotics against multidrug-resistant clinical strains of Pseudomonas aeruginosa. PLoS ONE 15(11):e0241304. https://doi.org/10.1371/journal.pone.0241304. (PMID: 10.1371/journal.pone.0241304331568387647105)
Withman B, Gunasekera TS, Beesetty P, Agans R, Paliy O (2013) Transcriptional responses of uropathogenic Escherichia coli to increased environmental osmolality caused by salt or urea. Infect Immun 81:80–89. https://doi.org/10.1128/iai.01049-12. (PMID: 10.1128/iai.01049-12230909573536127)
Wu J, Li Y, Xu B, Li M, Wang J, Shao Y, Chen F, Sun M, Liu B (2022) Effects of physicochemical parameters on struvite crystallization based on kinetics. Int J Environ Res Public Health 19:7204. https://doi.org/10.3390/ijerph19127204. (PMID: 10.3390/ijerph19127204357424539222832)
Yang H, Huang X, Zhang X, Zhang X, Xu X, She F, Wen Y (2022) AI-2 induces urease expression through downregulation of orphan response regulator HP1021 in Helicobacter pylori. Front Med 9:790994. https://doi.org/10.3389/fmed.2022.790994. (PMID: 10.3389/fmed.2022.790994)
Yuan F, Huang Z, Yang T, Wang G, Li P, Yang B, Li J (2021) Pathogenesis of Proteus mirabilis in catheter-associated urinary tract infections. Urol Int 105(5–6):354–361. https://doi.org/10.1159/000514097. (PMID: 10.1159/00051409733691318)
Yuvarajan S, Hameed A, Arun AB, Saptami K, Rekha PD (2022) Urease-negative uropathogen Kalamiella piersonii YU22 metabolizes urea by urea carboxylase and allophanate hydrolase enzyme system. Microbiol Res 263:127142. https://doi.org/10.1016/j.micres.2022.127142. (PMID: 10.1016/j.micres.2022.12714235940107)
Zhou C, Bhinderwala F, Lehman MK, Thomas VC, Chaudhari SS, Yamada KJ, Foster KW, Powers R, Kielian T, Fey PD (2019) Urease is an essential component of the acid response network of Staphylococcus aureus and is required for a persistent murine kidney infection. PLOS Pathog 15:e1007538. https://doi.org/10.1371/journal.ppat.1007538. (PMID: 10.1371/journal.ppat.1007538306089816343930)
Contributed Indexing: Keywords: Escherichia coli; Kidney stone disease; Pseudomonas aeruginosa; Urea metabolism; Urease activity; Urinary tract infection; ureC gene
Substance Nomenclature: EC 3.5.1.5 (Urease)
AW3EJL1462 (Struvite)
8W8T17847W (Urea)
Entry Date(s): Date Created: 20231116 Date Completed: 20231127 Latest Revision: 20231127
Update Code: 20260130
DOI: 10.1007/s00203-023-03722-6
PMID: 37973630
Database: MEDLINE
Description
ISSN:1432-072X
DOI:10.1007/s00203-023-03722-6