The Effect of Particulate Matter of Natural and Anthropogenic Origin on Growth Indicators and Sensitivity to Antibiotics of Escherichia coli B906

Authors

  • М.Yu. Korbush Taras Shevchenko National University of Kyiv, 64/13 Volodymyrska Str., Kyiv, 01601, Ukraine
  • Т.M. Serhiichuk Taras Shevchenko National University of Kyiv, 64/13 Volodymyrska Str., Kyiv, 01601, Ukraine
  • Y.M. Yumyna Taras Shevchenko National University of Kyiv, 64/13 Volodymyrska Str., Kyiv, 01601, Ukraine
  • T.O. Borisova Palladin Institute of Biochemistry, NAS of Ukraine, 9 Leontovycha Str., Kyiv, 01030, Ukraine
  • G.M. Tolstanova Taras Shevchenko National University of Kyiv, 64/13 Volodymyrska Str., Kyiv, 01601, Ukraine

DOI:

https://doi.org/10.15407/microbiolj85.04.034

Keywords:

particulate matter, air pollution, Escherichia coli, biofilm formation, antibiotic resistance, microbiota

Abstract

Particulate matter (PM), which is among the main components of polluted air, can contribute to the development of gastrointestinal diseases and alter the composition of gut microbiota and its metabolic properties. Objective. The study focuses on analyzing the influence of different concentrations of PM derived from the combustion of cottonwood (PMC) and medical masks (PMM) on the growth intensity, biofilm formation capability, and antibiotic susceptibility of lactose-positive Escherichia coli strain B906. Methods. The MPA medium was inoculated with a culture of E. coli B906 at a concentration of 105 CFU/mL, followed by the addition of PMC and PMM at concentrations of 18 μg/mL, 36 μg/mL, or 72 μg/mL. The growth intensity was determined by measuring the optical density using a spectrophotometer over a period of 72 h. To determine the number of viable cells and their ability to ferment lactose, seeding on the Endo medium was performed. The biofilm-forming ability was determined on polystyrene plates using a staining and desorption method. The antibiotic susceptibility (ampicillin, levomycetin, meropenem, norfloxacin, and ceftriaxone) was determined using the disc-diffusion method for 24, 48, and 72 h of cultivation. Results. Both PMC and PMM exerted suppressive effects on the growth of E. coli B906: at a concentration of 72 μg/mL, the biomass increase was virtually absent. The number of viable cells on the medium with PMC decreased by 1—2 orders of magnitude at concentrations of 18 μg/mL and 36 μg/mL compared to the control and by 6 orders of magnitude at a concentration of 72 μg/mL. At this concentration, no growth was observed at 48 and 72 h. PMM exerted bacteriostatic effects: when seeded on the Endo medium, the number of viable cells decreased by 1—2 orders of magnitude at concentrations of 18 μg/mL and 36 μg/mL from 24 to 72 h, and by 3—4 orders of magnitude at a concentration of 72 μg/mL. At 48 h cultivation, PMC stimulated biofilm formation at concentrations of 18 μg/mL and 36 μg/mL, while inhibiting it at a concentration of 72 μg/mL. In contrast, PMM reduced the biofilm density at all concentrations. Both types of PM induced resistance to ampicillin, but the effect was stronger for PMM, which also led to resistance to norfloxacin. Conclusions. This study demonstrates that both PMC and PMM have a direct impact on lactose-positive E. coli strain B906, reflected in decreased growth intensity at moderate and high concentrations (36 μg/mL and 72 μg/mL) and increased aggressiveness through reduced enzymatic activity, enhanced biofilm formation, and the emergence of resistance to ampicillin, ceftriaxone, and norfloxacin.

Downloads

Download data is not yet available.

References

How Does Air Pollution Affect Life Expectancy Around the World? A State of Global Air Special Report. Health Effects Institute; 2022.

Thangavel P, Park D, Lee YC. Recent insights into particulate matter (PM2.5)-mediated toxicity in humans: An overview. Int J Environ Res Public Health. 2022; 19(12):7511. https://doi.org/10.3390/ijerph19127511

Boogaard H, Walker K, Cohen AJ. Air pollution: the emergence of a major global health risk factor. Int Health. 2019; 11(6):417-421. https://doi.org/10.1093/inthealth/ihz078

Thurston GD, Kipen H, Annesi-Maesano I, et al. A joint ERS/ATS policy statement: what constitutes an adverse health effect of air pollution? An analytical framework. Eur Respir J. 2017; 49(1):1600419. https://doi.org/10.1183/13993003.00419-2016

Murray CJL, Aravkin AY, Zheng P, et al. Global burden of 87 risk factors in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Global burden of 87 risk factors in 204 countries and territories. 1990; 396:1223-1249.

Ambient (outdoor) air pollution. Accessed March 27, 2023. https://www.who.int/news-room/fact-sheets/detail/ambient-(outdoor)-air-quality-and-health

Baccarelli A, Martinelli I, Zanobetti A, et al. Exposure to particulate air pollution and risk of deep vein thrombosis. Arch Intern Med. 2008; 168(9):920-927. https://doi.org/10.1001/archinte.168.9.920

Brook RD, Rajagopalan S, Pope CA 3rd, et al. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation. 2010; 121(21):2331-2378. https://doi.org/10.1161/CIR.0b013e3181dbece1

Dai L, Zanobetti A, Koutrakis P, Schwartz JD. Associations of fine particulate matter species with mortality in the United States: a multicity time-series analysis. Environ Health Perspect. 2014; 122(8):837-842. https://doi.org/10.1289/ehp.1307568

Hamra GB, Guha N, Cohen A, et al. Outdoor particulate matter exposure and lung cancer: a systematic review and meta-analysis. Environ Health Perspect. 2014; 122(9):906-911. https://doi.org/10.1289/ehp/1408092

Paulin L, Hansel N. Particulate air pollution and impaired lung function. F1000Res. 2016; 5:201. https://doi.org/10.12688/f1000research.7108.1

Pambianchi E, Pecorelli A, Valacchi G. Gastrointestinal tissue as a 'new' target of pollution exposure. IUBMB Life. 2022; 74(1):62-73. https://doi.org/10.1002/iub.2530

Mutlu EA, Comba IY, Cho T, et al. Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ Pollut. 2018; 240:817- 830. https://doi.org/10.1016/j.envpol.2018.04.130

Kish L, Hotte N, Kaplan GG, et al. Environmental particulate matter induces Murine intestinal inflammatory responses and alters the gut microbiome. PLoS One. 2013; 8(4):e62220. https://doi.org/10.1371/journal.pone.0062220

Salim SY, Jovel J, Wine E, et al. Exposure to ingested airborne pollutant particulate matter increases mucosal exposure to bacteria and induces early onset of inflammation in neonatal IL-10-deficient mice. Inflamm Bowel Dis. 2014; 20(7):1129-1138. https://doi.org/10.1097/MIB.0000000000000066

Li N, Yang Z, Liao B, et al. Chronic exposure to ambient particulate matter induces gut microbial dysbiosis in a rat COPD model. Respir Res. 2020; 21(1):271. https://doi.org/10.1186/s12931-020-01529-3

Dorofeyev A, Dorofeyeva A, Borysov A, Tolstanova G, Borisova T. Gastrointestinal health: changes of intestinal mucosa and microbiota in patients with ulcerative colitis and irritable bowel syndrome from PM2. 5-polluted regions of Ukraine. Environmental Science and Pollution Research. 2023; 30(3):7312-7324. https://doi.org/10.1007/s11356-022-22710-9

Nicoletti M, Superti F, Conti C, Calconi A, Zagaglia C. Virulence factors of lactose-negative Escherichia coli strains isolated from children with diarrhea in Somalia. J Clin Microbiol. 1988; 26(3):524-529. https://doi.org/10.1128/jcm.26.3.524-529.1988

Hossain A. Presence and pattern of virulence genes in non-lactose fermenting Escherichia coli strains isolated from stools of children< 5 years in rural and urban Bangladesh. International Journal of Infectious Diseases. 2012; 16. https://doi.org/10.1016/j.ijid.2012.05.525

Mazumder R, Hussain A, Phelan JE, et al. Non-lactose fermenting Escherichia coli: Following in the footsteps of lactose fermenting E. coli high-risk clones. Front Microbiol. 2022; 13:1027494. https://doi.org/10.3389/fmicb.2022.1027494

Zhang T, Shi XC, Xia Y, Mai L, Tremblay PL. Escherichia coli adaptation and response to exposure to heavy atmospheric pollution. Sci Rep. 2019; 9(1):10879. https://doi.org/10.1038/s41598-019-47427-7

Paliienko K, Korbush M, Krisanova N, et al. Similar in vitro response of rat brain nerve terminals, colon preparations and COLO 205 cells to smoke particulate matter from different types of wood. Neurotoxicology. 2022; 93:244-256. https://doi.org/10.1016/j.neuro.2022.10.009

Saadat S, Rawtani D, Hussain CM. Environmental perspective of COVID-19. Sci Total Environ. 2020; 728(138870):138870. https://doi.org/10.1016/j.scitotenv.2020.138870

Borysov A, Tarasenko A, Krisanova N, et al. Plastic smoke aerosol: Nano-sized particle distribution, absorption/fluorescent properties, dysregulation of oxidative processes and synaptic transmission in rat brain nerve terminals. Environ Pollut. 2020; 263(Pt A):114502. https://doi.org/10.1016/j.envpol.2020.114502

Stepanović S, Vuković D, Hola V, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 2007; 115(8):891-899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x

On approval of methodological guidelines for determining the sensitivity of microorganisms to antibacterial drugs: Order of the Ministry of Health of Ukraine No. 167 of April 5, 2007. Accessed March 27, 2023. https://zakon.rada.gov.ua/rada/show/v0167282-07#Text

Gupta N, Yadav VK, Gacem A, et al. Deleterious Effect of Air Pollution on Human Microbial Community and Bacterial Flora: A Short Review. Int J Environ Res Public Health. 2022; 19(23):15494. https://doi.org/10.3390/ijerph192315494

Arrieta MC, Bistritz L, Meddings JB. Alterations in intestinal permeability. Gut. 2006; 55(10):1512-1520. https://doi.org/10.1136/gut.2005.085373

Verhaegh BPM, Bijnens EM, van den Heuvel TRA, et al. Ambient air quality as risk factor for microscopic colitis - A geographic information system (GIS) study. Environ Res. 2019; 178(108710):108710. https://doi.org/10.1016/j.envres.2019.108710

Parolisi R, Montarolo F, Pini A, Rovelli S, Cattaneo A, Bertolotto A. Exposure to fine particulate matter (PM25) hampers myelin repair in a mouse model of white matter demyelination. Neurochem Int. Published online 2021:442-445. https://doi.org/10.1016/j.neuint.2021.104991

Rhew SH, Kravchenko J, Lyerly HK. Exposure to low-dose ambient fine particulate matter PM25 and Alzheimer's disease, non-Alzheimer's dementia, and Parkinson's disease in North Carolina. PLoS ONE. 2021; 32:24-34.

Korbush M, Paliienko K, Dovbynchuk T, Borisova T, Tolstanova G. Particulate matter from natural precursor increases susceptibility to inflammatory bowel disease. UEG Week 2022 Poster Presentations. 2022; 10:620-621.

Zhang YJ, Li S, Gan RY, Zhou T, Xu DP, Li HB. Impacts of gut bacteria on human health and diseases. Int J Mol Sci. 2015; 16(4):7493-7519. https://doi.org/10.3390/ijms16047493

den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013; 54(9):2325-2340. https://doi.org/10.1194/jlr.R036012

Rossi E, Cimdins A, Lüthje P, et al. 'It's a gut feeling' -Escherichia coli biofilm formation in the gastrointestinal tract environment. Crit Rev Microbiol. 2018; 44(1):1-30. https://doi.org/10.1080/1040841X.2017.1303660

Sicard JF, Vogeleer P, Le Bihan G, et al. N-Acetyl-glucosamine influences the biofilm formation of Escherichia coli. Gut Pathog. 2018; 10:26. https://doi.org/10.1186/s13099-018-0252-y

Reygaert WC. An overview of the antimicrobial resistance mechanisms of bacteria. AIMS Microbiol. 2018; 4(3):482-501. https://doi.org/10.3934/microbiol.2018.3.482

Darby EM, Trampari E, Siasat P, et al. Molecular mechanisms of antibiotic resistance revisited. Nat Rev Microbiol. 2023; 21(5):280-295. https://doi.org/10.1038/s41579-022-00820-y

Blondeau JM. Fluoroquinolones: mechanism of action, classification, and development of resistance. Surv Ophthalmol. 2004; 49 Suppl 2(2):S73-8. https://doi.org/10.1016/j.survophthal.2004.01.005

Downloads

Published

2023-08-16

How to Cite

Korbush М., Serhiichuk Т., Yumyna, Y., Borisova, T., & Tolstanova, G. (2023). The Effect of Particulate Matter of Natural and Anthropogenic Origin on Growth Indicators and Sensitivity to Antibiotics of Escherichia coli B906. Mikrobiolohichnyi Zhurnal, 85(4), 34-45. https://doi.org/10.15407/microbiolj85.04.034
Received 2023-06-02
Accepted 2023-06-19
Published 2023-08-16