Secondary metabolite of Aspergillus oryzae impairs cell envelope integrity Klebsiella pneumoniae producing extended-spectrum beta-lactamase

Lailia Nur Rachma; Loeki Enggar Fitri; Sumarno Reto Prawiro; Tri Yudani Mardining Raras

doi:10.7324/JAPS.2023.106333

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Abstract

The defense system of Klebsiella pneumoniae producing extended-spectrum beta-lactamase (KPESBL) against the environment depends on the cell envelope and capsular polysaccharide (CPS). Its integrity depends on peptidoglycan-associated lipoprotein (pal), murein lipoprotein (lpp), and outer membrane protein A (ompA) covered by CPS. The outer membrane protects the cell envelope and serves as a siderophore entry-exit channel and membrane anchor for the CPS and fimbriae, crucial for K. pneumoniae pathogenicity. Here, we describe the effects of the secondary metabolite of Aspergillus oryzae (SMAO) on cell envelope integrity, cell adhesion, CPSs, siderophore, and KPESBL proliferation. The SMAO was exposed to the strain (KPESBL). Using quantitative real-time polymerase chain reaction, the expression of the pal, lpp, and ompA genes was assessed; CPS levels were measured using the Congo red binding assay (CR). Siderophore was measured using the chrome azurol sulphonate assay. Bacterial cell adherence was measured using the yeast agglutination assay. The growth curve was measured using the microdilution method. As validation, scanning electron microscopy was used to examine the structure of the cell membrane following exposure to SMAO. SMAO impairs the integrity of the cell envelope of KPESBL. Our research shows that SMAO may be a possible anti-infectious drug that breaks down the integrity of the cell envelope.

Citation:

Rachma LN, Fitri LE, Prawiro SR, Raras TYM. Secondary metabolite of Aspergillus oryzae impairs cell envelope integrity Klebsiella pneumoniae producing extended-spectrum beta-lactamase. J Appl Pharm Sci, 2023; 13(06):137–145. https://doi.org/10.7324/JAPS.2023.106333

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Baker JL, Hendrickson EL, Tang X, Lux R, He X, Edlund A, McLean JS, Shi W. Klebsiella and Providencia emerge as lone survivors following long-term starvation of oral microbiota. Proc Natl Acad Sci, 2019; 116(17):8499-504; doi: 10.1073/pnas.1820594116 https://doi.org/10.1073/pnas.1820594116
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Duong-Ly KC, Gabelli SB. Salting out of proteins using ammonium sulfate precipitation. Methods Enzymol, 2014; 541:85-94; doi: 10.1016/B978-0-12-420119-4.00007-0 https://doi.org/10.1016/B978-0-12-420119-4.00007-0
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Alsharif W, Saad MM, Hirt H. Desert microbes for boosting sustainable agriculture in extreme environments. Front Microbiol, 2020; 11:1666; doi: 10.3389/fmicb.2020.01666 https://doi.org/10.3389/fmicb.2020.01666

Baker JL, Hendrickson EL, Tang X, Lux R, He X, Edlund A, McLean JS, Shi W. Klebsiella and Providencia emerge as lone survivors following long-term starvation of oral microbiota. Proc Natl Acad Sci, 2019; 116(17):8499-504; doi: 10.1073/pnas.1820594116 https://doi.org/10.1073/pnas.1820594116

Breurec S, Melot B, Hoen B, Passet V, Schepers K, Bastian S, Brisse S. Liver abscess caused by infection with community-acquired Klebsiella quasipneumoniae subsp. Quasipneumoniae. Emerg Infect Dis, 2016; 22(3):529-31; doi: 10.3201/eid2203.151466 https://doi.org/10.3201/eid2203.151466

Caza M, Kronstad JW. Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol, 2013; 3; doi: 10.3389/fcimb.2013.00080 https://doi.org/10.3389/fcimb.2013.00080

Chen T, Dong G, Zhang S, Zhang X, Zhao Y, Cao J, Zhou T, Wu Q. Effects of iron on the growth, biofilm formation and virulence of Klebsiella pneumoniae causing liver abscess. BMC Microbiol, 2020; 20(1):36; doi: 10.1186/s12866-020-01727-5 https://doi.org/10.1186/s12866-020-01727-5

Cress BF, Englaender JA, He W, Kasper D, Linhardt RJ, Koffas MAG. Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules. FEMS Microbiol Rev, 2014; 38(4):660-97; doi: 10.1111/1574-6976.12056 https://doi.org/10.1111/1574-6976.12056

Culler H, Couto S, Higa J, Ruiz R, Yang M, Bueris V, Franzolin M, Sircili M. Role of SdiA on biofilm formation by atypical enteropathogenic Escherichia coli. Genes, 2018; 9(5):253; doi: 10.3390/genes9050253 https://doi.org/10.3390/genes9050253

Duong-Ly KC, Gabelli SB. Salting out of proteins using ammonium sulfate precipitation. Methods Enzymol, 2014; 541:85-94; doi: 10.1016/B978-0-12-420119-4.00007-0 https://doi.org/10.1016/B978-0-12-420119-4.00007-0

Flipphi M, Sun J, Robellet X, Karaffa L, Fekete E, Zeng AP, Kubicek CP. Biodiversity and evolution of primary carbon metabolism in Aspergillus nidulans and other Aspergillus spp. Fungal Genet Biol, 2009; 46(1):S19-44; doi: 10.1016/j.fgb.2008.07.018 https://doi.org/10.1016/j.fgb.2008.07.018

Gharrah MM, El-Mahdy AM, Barwa RF. Association between virulence factors and extended spectrum beta-lactamase producing Klebsiella pneumoniae compared to nonproducing isolates. Interdiscip Perspect Infect Dis, 2017:7279830; doi: 10.1155/2017/7279830. https://doi.org/10.1155/2017/7279830

Graham CLB, Newman H, Gillett FN, Smart K, Briggs N, Banzhaf M, Roper DI. A dynamic network of proteins facilitate cell envelope biogenesis in Gram-negative bacteria. Int J Mol Sci, 2021; 22(23):12831; doi: 10.3390/ijms222312831 https://doi.org/10.3390/ijms222312831

Gunther NW, Lockatell V, Johnson DE, Mobley HLT. In vivo dynamics of type 1 fimbria regulation in uropathogenic Escherichia coli during experimental urinary tract infection. Infect Immun, 2001; 69(5):2838-46; doi: 10.1128/IAI.69.5.2838-2846.2001 https://doi.org/10.1128/IAI.69.5.2838-2846.2001

Guo R, Luo X, Liu J, Lu H. Mass spectrometry based targeted metabolomics precisely characterized new functional metabolites that regulate biofilm formation in Escherichia coli. Anal Chim Acta, 2021; 1145:26-36; doi: 10.1016/j.aca.2020.12.021 https://doi.org/10.1016/j.aca.2020.12.021

Hellman J, Loiselle PM, Tehan MM, Allaire JE, Boyle LA, Kurnick JT, Andrews DM, Sik KK, Warren HS. Outer membrane protein a, peptidoglycan-associated lipoprotein, and murein lipoprotein are released by Escherichia coli bacteria into serum. Infect Immun, 2000; 68(5):2566- 72; doi: 10.1128/IAI.68.5.2566-2572.2000 https://doi.org/10.1128/IAI.68.5.2566-2572.2000

Houda SN, Rachid B, Julio G, Jesus RSM, Teresa V. In vitro antimicrobial, antiviral and cytotoxicity activities of Aspergillus oryzae isolated from El-Baida Marsh in Algeria. J Drug Deliv Ther, 2020; 10(4):191-5; doi: 10.22270/jddt.v10i4.4261 https://doi.org/10.22270/jddt.v10i4.4261

Hsieh PF, Liu JY, Pan YJ, Wu MC, Lin TL, Huang YT, Wang JT. Klebsiella pneumoniae peptidoglycan-associated lipoprotein and murein lipoprotein contribute to serum resistance, antiphagocytosis, and proinflammatory cytokine stimulation. J Infect Dis, 2013; 208(10):1580-9; doi: 10.1093/infdis/jit384 https://doi.org/10.1093/infdis/jit384

Jahn CE, Charkowski AO, Willis DK. Evaluation of isolation methods and RNA integrity for bacterial RNA quantitation. J Microbiol Methods, 2008; 75:318-24. doi: 10.1016/j.mimet.2008.07.004 https://doi.org/10.1016/j.mimet.2008.07.004

Jiao L, Li J, Liu F, Wang J, Jiang P, Li B, Li H, Chen C, Wu W. Characterisation, chain conformation and antifatigue effect of steamed ginseng polysaccharides with different molecular weight. Front Pharmacol, 2021; 12:712836; doi: 10.3389/fphar.2021.712836 https://doi.org/10.3389/fphar.2021.712836

Khatoon Z, McTiernan CD, Suuronen EJ, Mah TF, Alarcon EI. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon, 2018; 4(12):e01067; doi: 10.1016/j. heliyon.2018.e01067 https://doi.org/10.1016/j.heliyon.2018.e01067

Lee KJ, Kim JA, Hwang W, Park SJ, Lee KH. Role of capsular polysaccharide (CPS) in biofilm formation and regulation of CPS production by quorum-sensing in Vibrio vulnificus: quorum-sensing represses CPS production and biofilm. Mol Microbiol, 2013; 90(4):841-57; doi: 10.1111/mmi.12401 https://doi.org/10.1111/mmi.12401

Lee CH, Su LH, Liu JW, Chang CC, Chen RF, Yang KD. Aspirin enhances opsonophagocytosis and is associated to a lower risk for Klebsiella pneumoniaeinvasive syndrome. BMC Infect Dis, 2014; 14(1):47; doi: 10.1186/1471-2334-14-47 https://doi.org/10.1186/1471-2334-14-47

Lin TH, Huang SH, Wu CC, Liu HH, Jinn TR, Chen Y, Lin CT. Inhibition of Klebsiella pneumoniae growth and capsular polysaccharide biosynthesis by Fructus mume. Evid Based Complement Alternat Med, 2013:1-10; doi: 10.1155/2013/621701 https://doi.org/10.1155/2013/621701

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 2001:402-8; doi: 10.1006/meth.2001.1262. https://doi.org/10.1006/meth.2001.1262

Misra S, Sharma V, Srivastava AK. Bacterial polysaccharides: an overview. In: Ramawat KG, Mérillon JM (Eds.). Polysaccharides, Springer International Publishing, 2014; doi: 10.1007/978-3-319-03751-6_68-1 https://doi.org/10.1007/978-3-319-03751-6_68-1

Mol O, Oudega B. Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol Rev, 1996; 19(1):25-52; doi: 10.1111/j.1574-6976.1996.tb00252.x https://doi.org/10.1111/j.1574-6976.1996.tb00252.x

Nacef HS, Belhattab R, Larous L. Chemical composition, antimicrobial study against human and plant pathogenic microorganisms and optimization of bioactive metabolites produced by the new strain Aspergillus oryzae 18HG80 isolated from saline soil (El-Baida Marsh, Algeria). J Microbiol Res, 2020; 10:11-21.

Navon-Venezia S, Kondratyeva K, Carattoli A. Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol Rev, 2017; 41(3):252-75; doi: 10.1093/femsre/fux013 https://doi.org/10.1093/femsre/fux013

Nevermann J, Silva A, Otero C, Oyarzún DP, Barrera B, Gil F, Calderón IL, Fuentes JA. Identification of genes involved in biogenesis of outer membrane vesicles (OMVs) in Salmonella enterica Serovar Typhi. Front Microbiol, 2019; 10:104; doi: 10.3389/fmicb.2019.00104 https://doi.org/10.3389/fmicb.2019.00104

Pacheco T, Gomes AÉI, Siqueira NMG, Assoni L, Darrieux M, Venter H, Ferraz LFC. SdiA, a quorum-sensing regulator, suppresses fimbriae expression, biofilm formation, and quorum-sensing signaling molecules production in Klebsiella pneumoniae. Front Microbiol, 2021; 12:597735; doi: 10.3389/fmicb.2021.597735 https://doi.org/10.3389/fmicb.2021.597735

Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the offense with a strong defense. Microbiol Mol Biol Rev, 2016; 80(3):629- 61; doi: 10.1128/MMBR.00078-15 https://doi.org/10.1128/MMBR.00078-15

Rachma LN, Fitri LE, Prawiro SR, Raras TYM. Aspergillus oryzae attenuates quorum sensing-associated virulence factors and biofilm formation in Klebsiella pneumoniae extended-spectrum beta-lactamases. F1000Research, 2022; 11(1148):1148. https://doi.org/10.12688/f1000research.123391.1

Schwechheimer C, Sullivan CJ, Kuehn MJ. Envelope control of outer membrane vesicle production in Gram-negative bacteria. Biochemistry, 2013; 52(18):3031-40; doi: 10.1021/bi400164t https://doi.org/10.1021/bi400164t

Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol, 2015; 13(10):605-19; doi: 10.1038/nrmicro3525 https://doi.org/10.1038/nrmicro3525

Sinha AK, Venkateswaran BP, Tripathy SC, Sarkar A, Prabhakaran S. Effects of growth conditions on siderophore producing bacteria and siderophore production from Indian Ocean sector of Southern Ocean. J Basic Microbiol, 2019; 59(4):412-24; doi: 10.1002/ jobm.201800537 https://doi.org/10.1002/jobm.201800537

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