In vitro antibacterial and anti-biofilm potential of an endophytic Schizophyllum commune.
Anti-biofilm
Antibacterial
Basidiomycetes
Endophyte
Schizophyllum commune
Journal
AMB Express
ISSN: 2191-0855
Titre abrégé: AMB Express
Pays: Germany
ID NLM: 101561785
Informations de publication
Date de publication:
20 Jan 2024
20 Jan 2024
Historique:
received:
13
06
2023
accepted:
07
01
2024
medline:
21
1
2024
pubmed:
21
1
2024
entrez:
20
1
2024
Statut:
epublish
Résumé
The emergence of antibiotic resistance in pathogens is one of the major health concerns facing mankind as different bacterial strains have developed resistance to antibiotics over the period of time due to overuse and misuse of antibiotics. Besides this, ability to form biofilms is another major factor contributing to antibiotic resistance, which has necessitated the need for exploration for novel and effective compounds with ability to inhibit biofilm formation. Endophytic fungi are reported to exhibit antibacterial and anti-biofilm potential and could serve as a potent source of novel antibacterial compounds. Majority of the bioactivities have been reported from fungi belonging to phylum Ascomycota. Endophytic basidiomycetes, inspite of their profound ability to serve as a source of bioactive compounds have not been exploited extensively. In present study, an attempt was made to assess the antibacterial, anti-biofilm and biofilm dispersion potential of an endophytic basidiomycetous fungus Schizophyllum commune procured from the culture collection of our lab. Ethyl acetate extract of S. commune showed good antibacterial activity against Staphylococcus aureus, Klebsiella pneumoniae, Escherichia coli, Pseudomonas aeruginosa, Salmonella enterica and Vibrio cholerae. Minimum inhibitory concentration and minimum bactericidal concentration of the extract were in the range of 1.25-10 mg/ml against the tested bacterial pathogens. The mode of action was determined to be bactericidal which was further confirmed by time kill studies. Good anti-biofilm activity of S. commune extract was recorded against K. pneumoniae and S. enterica, which was further validated by fluorescence microscopy. The present study highlights the importance of endophytic basidiomycetes as source of therapeutic compounds.
Identifiants
pubmed: 38245627
doi: 10.1186/s13568-024-01663-x
pii: 10.1186/s13568-024-01663-x
doi:
Types de publication
Journal Article
Langues
eng
Pagination
10Informations de copyright
© 2024. The Author(s).
Références
Achika JI, Ayo RG, Habila JD, Oyewale AO (2020) Terpenes with antimicrobial and antioxidant activities from Lannea Humilis (Oliv). Sci Afr 10:e00552
Allocati N, Masulli M, Alexeyev MF, Di Ilio C (2013) Escherichia coli in Europe: an overview. Int J Environ Res Public Health 10(12):6235–6254
pubmed: 24287850
pmcid: 3881111
doi: 10.3390/ijerph10126235
Almagro-Moreno S, Taylor RK (2013) Cholera: environmental reservoirs and impact on disease transmission. Microbiol Spectr 1(2):1–2
doi: 10.1128/microbiolspec.OH-0003-2012
Alves MJ, Ferreira IC, Froufe HJ, Abreu RMV, Martins A, Pintado M (2013) Antimicrobial activity of phenolic compounds identified in wild mushrooms, SAR analysis and docking studies. J Appl Microbiol 115(2):346–357
pubmed: 23510516
doi: 10.1111/jam.12196
Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48:5–16
pubmed: 11420333
doi: 10.1093/jac/48.suppl_1.5
Appiah T, Boakye YD, Agyare C (2017) Antimicrobial activities and time-kill kinetics of extracts of selected Ghanaian mushrooms. Evid Based Complement Alternat Med 2017:1–15
doi: 10.1155/2017/4534350
Arun G, Eyini M, Gunasekaran P (2015) Characterization and biological activities of extracellular melanin produced by Schizophyllum commune (fries). Indian J Exp Biol 53:380–387
pubmed: 26155678
CDC (2019) Antibiotic resistance threats in the United States. Atlanta, GA: U.S. Department of Health and Human Services CDC 2019
Chen GG, Zhu QF, Long XM, Lu Q, Li KY, Chen Q, Zhou M, Liao SG, Xu GB (2021) Antibacterial activities of the chemical constituents of Schizophyllum commune MST7-3 collected from coal area. Nat Prod Res 36(18):4645–4654
doi: 10.1080/14786419.2021.2010075
Crowley LC, Scott AP, Marfell BJ, Boughaba JA, Chojnowski G, Waterhouse NJ (2016) Measuring cell death by propidium iodide uptake and flow cytometry. Cold Spring Harb Protoc 2016(7):647–651
doi: 10.1101/pdb.prot087163
Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74(3):417–433
pubmed: 20805405
pmcid: 2937522
doi: 10.1128/MMBR.00016-10
Dayan GH, Mohamed N, Scully IL, Cooper D, Begier E, Eiden J, Jansen KU, Gurtman A, Anderson AS (2016) Staphylococcus aureus: the current state of disease, pathophysiology and strategies for prevention. Expert Rev Vaccines 15(11):1373–1392
pubmed: 27118628
doi: 10.1080/14760584.2016.1179583
Deka AC, Sarma I, Dey S, Sarma TC (2017) Antimicrobial properties and phytochemical screening of some wild macrofungi of Rani-Garbhanga reserve forest area of Assam, India. Adv Appl Sci Res 8(3):17–22
Deshmukh SK, Verekar SA, Bhave SV (2015) Endophytic fungi: a reservoir of antibacterials. Front Microbiol 5:715
pubmed: 25620957
pmcid: 4288058
doi: 10.3389/fmicb.2014.00715
Deshmukh SK, Dufossé L, Chhipa H, Saxena S, Mahajan GB, Gupta MK (2022) Fungal endophytes: a potential source of antibacterial compounds. J Fungi 8(2):164
doi: 10.3390/jof8020164
Ditamo Y, Rupil LL, Sendra VG, Nores GA, Roth GA, Irazoqui FJ (2016) In vivo immunomodulatory effect of the lectin from edible mushroom Agaricus bisporus. Food Funct 7(1):262–269
Du B, Yang Y, Bian Z, Xu B (2017) Characterization and anti-inflammatory potential of an exopolysaccharide from submerged mycelial culture of Schizophyllum commune. Front Pharmacol 8:252
pubmed: 28555107
pmcid: 5430044
doi: 10.3389/fphar.2017.00252
Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH (2015) Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci 8(3):284–293
doi: 10.1080/21553769.2015.1051243
Farhat H, Urooj F, Tariq A, Sultana V, Ansari M, Ahmad VU, Ehteshamul-Haque S (2019) Evaluation of antimicrobial potential of endophytic fungi associated with healthy plants and characterization of compounds produced by endophytic Cephalosporium and Fusarium solani. Biocatal Agric Biotechnol 18:101043
doi: 10.1016/j.bcab.2019.101043
Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14(9):563–575
pubmed: 27510863
doi: 10.1038/nrmicro.2016.94
Guimarães AC, Meireles LM, Lemos MF, Guimarães MCC, Endringer DC, Fronza M, Scherer R (2019) Antibacterial activity of terpenes and terpenoids present in essential oils. Molecules 24(13):2471
pubmed: 31284397
pmcid: 6651100
doi: 10.3390/molecules24132471
Guzmán G (2008) Diversity and use of traditional Mexican medicinal fungi. A review. Int J Med Mushrooms 10(3):209–217
doi: 10.1615/IntJMedMushr.v10.i3.20
Harrell JE, Hahn MM, D’Souza SJ, Vasicek EM, Sandala JL, Gunn JS, McLachlan JB (2021) Salmonella biofilm formation, chronic infection, and immunity within the intestine and hepatobiliary tract. Front Cell Infect Microbiol 10:624622
pubmed: 33604308
pmcid: 7885405
doi: 10.3389/fcimb.2020.624622
Jiao C, Xie YZ, Yang X, Li H, Li XM, Pan HH, Cai MH, Zhong HM, Yang BB (2013) Anticancer activity of Amauroderma rude. PLoS ONE 8(6):e66504
pubmed: 23840494
pmcid: 3688780
doi: 10.1371/journal.pone.0066504
Johnson JR, Stell AL (2000) Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181(1):261–272
pubmed: 10608775
doi: 10.1086/315217
Joshi S, Bisht GS, Rawat DS, Kumar A, Kumar R, Maiti S, Pasha S (2010) Interaction studies of novel cell selective antimicrobial peptides with model membranes and E. coli ATCC 11775. Biochim Biophys Acta 1798(10):1864–1875
pubmed: 20599694
doi: 10.1016/j.bbamem.2010.06.016
Kalia V, Miglani R, Purnapatre KP, Mathur T, Singhal S, Khan S, Voleti SR, Upadhyay DJ, Saini KS, Rattan A, Raj VS (2009) Mode of action of ranbezolid against staphylococci and structural modeling studies of its interaction with ribosomes. Antimicrob Agents Chemother 53(4):1427–1433
pubmed: 19075051
doi: 10.1128/AAC.00887-08
Kamalebo HM, Malale HNSW, Ndabaga CM, Degreef J, De Kesel A (2018) Uses and importance of wild fungi: traditional knowledge from the Tshopo province in the Democratic Republic of the Congo. J Ethnobiol Ethnomed 14(1):1–12
Kaur S, Sharma P (2015) Protease-sensitive inhibitory activity of cell-free supernatant of Lactobacillus crispatus 156 synergizes with ciprofloxacin, moxifloxacin and streptomycin against Pseudomonas aeruginosa: an in vitro study. Probiotics Antimicrob Proteins 7:172–180
pubmed: 25693845
doi: 10.1007/s12602-015-9188-4
Kaur S, Sharma P, Kalia N, Singh J, Kaur S (2018) Anti-biofilm properties of the fecal probiotic lactobacilli against Vibrio Spp. Front Cell Infect Microbiol 8:120
pubmed: 29740541
pmcid: 5928150
doi: 10.3389/fcimb.2018.00120
Kaur J, Dhama AS, Buttolia H, Kaur J, Walia K, Ohri V, Kumar V, Lynn AM, Srivastava A, Singh H (2021) ICMR’s antimicrobial resistance surveillance system (i-AMRSS): a promising tool for global antimicrobial resistance surveillance. JAC Antimicrob Resist 3(1):1–6
doi: 10.1093/jacamr/dlab023
Keepers TR, Gomez M, Celeri C, Nichols WW, Krause KM (2014) Bactericidal activity, absence of serum effect, and time-kill kinetics of ceftazidime-avibactam against β-lactamase-producing Enterobacteriaceae and Pseudomonas aeruginosa. Antimicrob Agents Chemother 58(9):5297–5305
pubmed: 24957838
pmcid: 4135815
doi: 10.1128/AAC.02894-14
Khatoon Z, McTiernan CD, Suuronen EJ, Mah TF, Alarcon EI (2018) Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon 4(12):e01067
pubmed: 30619958
pmcid: 6312881
doi: 10.1016/j.heliyon.2018.e01067
Kou RW, Du ST, Xia B, Zhang Q, Yin X, Gao JM (2021) Phenolic and steroidal metabolites from the cultivated edible Inonotus hispidus mushroom and their bioactivities. J Agric Food Chem 69(2):668–675
pubmed: 33398984
doi: 10.1021/acs.jafc.0c06822
López Romo A, Quirós R (2019) Appropriate use of antibiotics: an unmet need. Ther Adv Urol 11:9–17
doi: 10.1177/1756287219832174
Lowy FD (2003) Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest 111(9):1265–1273
pubmed: 12727914
pmcid: 154455
doi: 10.1172/JCI18535
Luís Â, Silva F, Sousa S, Duarte AP, Domingues F (2014) Antistaphylococcal and biofilm inhibitory activities of gallic, caffeic, and chlorogenic acids. Biofouling 30(1):69–79
pubmed: 24228999
doi: 10.1080/08927014.2013.845878
MacGowan A, Macnaughton E (2017) Antibiotic resistance. Medicine 45(10):622–628
doi: 10.1016/j.mpmed.2017.07.006
Maddox CE, Laur LM, Tian L (2010) Antibacterial activity of phenolic compounds against the phytopathogen Xylella fastidiosa. Curr Microbiol 60:53–58
pubmed: 19813054
doi: 10.1007/s00284-009-9501-0
Mayakrishnan V, Abdullah N, Abidin MHZ, Fadzil NHM, Johari NMK, Aminudin N, Abidin NZ (2013) Investigation of the antioxidative potential of various solvent fractions from fruiting bodies of Schizophyllum commune (Fr.) Mushrooms and characterization of phytoconstituents. J Agric Sci 5(6):58–68
Mbekou MIK, Dize D, Yimgang VL, Djague F, Toghueo RMK, Sewald N, Lenta BN, Boyom FF (2021) Antibacterial and mode of action of extracts from endophytic fungi derived from Terminalia mantaly, Terminalia catappa, and Cananga odorata. Biomed Res Int 2021:1–13
doi: 10.1155/2021/6697973
Miklasińska-Majdanik M, Kępa M, Wojtyczka RD, Idzik D, Wąsik TJ (2018) Phenolic compounds diminish antibiotic resistance of Staphylococcus aureus clinical strains. Int J Environ Res Public Health 15(10):2321
pubmed: 30360435
pmcid: 6211117
doi: 10.3390/ijerph15102321
Mogana R, Adhikari A, Tzar MN, Ramliza R, Wiart C (2020) Antibacterial activities of the extracts, fractions and isolated compounds from Canarium patentinervium Miq.against bacterial clinical isolates. BMC Complement Med Ther 20(1):1–11
doi: 10.1186/s12906-020-2837-5
Navon-Venezia S, Kondratyeva K, Carattoli A (2017) Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol Rev 41(3):252–275
pubmed: 28521338
doi: 10.1093/femsre/fux013
Parvekar P, Palaskar J, Metgud S, Maria R, Dutta S (2020) The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of silver nanoparticles against Staphylococcus aureus. Biomater Investig Dent 7(1):105–109
pubmed: 32939454
pmcid: 7470068
Pulingam T, Parumasivam T, Gazzali AM, Sulaiman AM, Chee JY, Lakshmanan M, Chin CF, Sudesh K (2022) Antimicrobial resistance: prevalence, economic burden, mechanisms of resistance and strategies to overcome. Eur J Pharm Sci 170:106103
pubmed: 34936936
doi: 10.1016/j.ejps.2021.106103
Rahman SFSA, Sijam K, Omar D (2014) Identification and antibacterial activity of phenolic compounds in crude extracts of Piper Sarmentosum (Kadok). J Pure Appl Microbiol 8(2):483–490
Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research. Springer, Cham
Rather MA, Gupta K, Bardhan P, Borah M, Sarkar A, Eldiehy KS, Bhuyan S, Mandal M (2021) Microbial biofilm: A matter of grave concern for human health and food industry. J Basic Microbiol 61(5):380–395
pubmed: 33615511
doi: 10.1002/jobm.202000678
Raut JS, Shinde RB, Chauhan NM, Mohan Karuppayil S (2013) Terpenoids of plant origin inhibit morphogenesis, adhesion, and biofilm formation by Candida albicans. Biofouling 29(1):87–96
pubmed: 23216018
doi: 10.1080/08927014.2012.749398
Rustamova N, Gao Y, Zhang Y, Yili A (2020) Biological activity of endophytic fungi from the roots of the medicinal plant Vernonia anthelmintica. Microorganisms 8(4):586
pubmed: 32316675
pmcid: 7232482
doi: 10.3390/microorganisms8040586
Schulze A, Mitterer F, Pombo JP, Schild S (2021) Biofilms by bacterial human pathogens: clinical relevance-development, composition and regulation-therapeutical strategies. Microb Cell 8(2):28–56
pubmed: 33553418
pmcid: 7841849
doi: 10.15698/mic2021.02.741
Sharma D, Misba L, Khan AU (2019) Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control 8(1):1–10
doi: 10.1186/s13756-019-0533-3
Sharma P, Rashid M, Kaur S (2020) Novel enterocin E20c purified from Enterococcus hirae 20c synergised with ß-lactams and ciprofloxacin against Salmonella enterica. Microb Cell Factories 19(1):1–11
doi: 10.1186/s12934-020-01352-x
Sharma A, Kaur R, Kaur J, Garg S, Bhatti R, Kaur A (2021) An endophytic Schizophyllum commune Fr. exhibits in-vitro and in-vivo antidiabetic activity in streptozotocin induced diabetic rats. AMB Express 11:1–11
Singh B, Singh S (2003) Antimicrobial activity of terpenoids from Trichodesma Amplexicaule Roth. Phytother Res 17(7):814–816
pubmed: 12916085
doi: 10.1002/ptr.1202
Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292(2):107–113
pubmed: 12195733
doi: 10.1078/1438-4221-00196
Sumayya SS, Lubaina AS, Murugan K (2020) Bactericidal potentiality of purified terpenoid extracts from the selected sea weeds and its mode of action. J Trop Life Sci 10(3):197–205
Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr (2015) Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 28(3):603–661
pubmed: 26016486
pmcid: 4451395
doi: 10.1128/CMR.00134-14
Tripathi AM, Tiwary BN (2013) Biochemical constituents of a wild strain of Schizophyllum commune isolated from Achanakmar-Amarkantak Biosphere Reserve (ABR), India. World J Microbiol Biotechnol 29:1431–1442
pubmed: 23475305
doi: 10.1007/s11274-013-1306-4
Tyagi B, Dubey A, Verma AK, Tiwari S (2015) Antibacterial activity of phenolics compounds against pathogenic bacteria. Int J Pharm Sci Rev Res 35(1):16–18
Vestby LK, Grønseth T, Simm R, Nesse LL (2020) Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics 9(2):59
pubmed: 32028684
pmcid: 7167820
doi: 10.3390/antibiotics9020059
Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73(2):274–276
doi: 10.2307/3545919
Wolf P, Elsässer-Beile U (2009) Pseudomonas exotoxin A: from virulence factor to anti-cancer agent. Int J Med Microbiol 299(3):161–176
pubmed: 18948059
doi: 10.1016/j.ijmm.2008.08.003
Yang SK, Yusoff K, Ajat M, Yap WS, Lim SHE, Lai KS (2021) Antimicrobial activity and mode of action of terpene linalyl anthranilate against carbapenemase-producing Klebsiella pneumoniae. J Pharm Anal 11(2):210–219
pubmed: 34012697
doi: 10.1016/j.jpha.2020.05.014
Yim HS, Chye FY, Rao V, Low JY, Matanjun P, How SE, Ho CW (2013) Optimization of extraction time and temperature on antioxidant activity of Schizophyllum commune aqueous extract using response surface methodology. J Food Sci Technol 50:275–283
pubmed: 24425917
doi: 10.1007/s13197-011-0349-5
Zaman SB, Hussain MA, Nye R, Mehta V, Mamun KT, Hossain N (2017) A review on antibiotic resistance: alarm bells are ringing. Cureus 9(6):1–9