Biosynthesis and antibacterial characterization of silver nanoparticles derived from streptomyces associated with crinum latifolium l

VIETNAM NATIONAL UNIVERSITY OF AGRICULTURE FACULTY OF BIOTECHNOLOGY  GRADUATION THESIS TITLE: “BIOSYNTHESIS AND ANTIBACTERIAL CHARACTERIZATION OF SILVER NANOPARTICLES DERIVED FROM STREPTOMYCES ASSOCIATED WITH CRINUM LATIFOLIUM L.” Hanoi - 2023 VIETNAM NATIONAL UNIVERSITY OF AGRICULTURE FACULTY OF BIOTECHNOLOGY  GRADUATION THESIS TITLE: “BIOSYNTHESIS AND ANTIBACTERIAL CHARACTERIZATION OF SILVER NANOPARTICLES DERIVED FROM STREPTOMYCES ASSOCIATED WITH CRINUM LATIFOLIUM L.” Student name : DINH THI LINH CHI Class : K63CNSHE Student’s code : 637406 Supervisor : QUACH NGOC TUNG, Ph.D NGUYEN THANH HUYEN, Msc Department : MICROBIAL BIOTECHNOLOGY Hanoi - 2023 COMMITMENT I hereby declare that the data and results stated in the thesis are honest and have never been published by anyone in other studies In the references section, the graduations with references to papers and action information are mentioned I am completely responsible for the data of this thesis Hanoi, January 9th, 2023 Sincerely Dinh Thi Linh Chi i ACKNOWLEDGEMENTS First and foremost, I would like to express my heartfelt gratitude to my main supervisor Dr Quach Ngoc Tung from VAST - Culture Collection of Microorganisms (VCCM), Institute of Biotechnology, Vietnam Academy of Science and Technology The inspiration, valuable guidance, and support he provided was vital driving force behind the theiss, which helped me to achieve the best and strive towards my goals I would also like to thank Msc Nguyen Thanh Huyen, a Vice head of the Department of Microbial biotechnology at the Vietnam National University of Agriculture, for co-supervising the thesis, for giving me the golden opportunity to work at VCCM and keeping me on track A special thank you to Assoc Prof Phi Quyet Tien, Ph.D Vu Thi Hanh Nguyen, and researchers at the VCCM-Institute of Biotechnology, who have provided technical support and imparted valuable knowledge as well as research experience The knowledge and skills gained would be beneficial in the future it had been a warm and fruitful experience Without the immense support of the Board of Directors at Vietnam National University of Agriculture and the lecturers of Biotechnology Department, Vietnam National University of Agriculture, I would not have been able to acquire the professional foundation necessary to complete this report, and the wealth of experience that has helped me take my first confident steps along my chosen career path Thank you too to all my friends in the laboratory who have made coming to VCCM so enjoyable The research leading to these results has received funding from Vietnam Academy of Science and Technology under grant agreement no ĐLTE00.03/21-22 To wrap up, I'd want to express my gratitude to my family and all who have journeyed with me, encouraged me, and shared in my experiences I sincerely thank you! Hanoi, Janury 9th, 2023 Sincerely Dinh Thi Linh Chi ii TABLE OF CONTENTS COMMITMENT i ACKNOWLEDGEMENTS ii TABLE OF CONTENTS iii LIST OF TABLES v LIST OF FIGURES vi LIST OF ABBREVIATIONS vii ABSTRACT viii I INTRODUCTION II LITERATURE REVIEW 2.1 Overview of silver nanoparticles 2.1.1 Nanoparticles 2.1.2 Silver nanoparticles and their characteristics .3 2.1.3 Applications of silver nanoparticles .5 2.2 Synthesis of silver nanoparticles 2.2.1 Chemical and physical synthesis 2.2.2 Green synthesis of silver nanoparticles 2.3 Modes of action against microorganisms of silver nanoparticles 2.3.1 Antimicrobial properties .8 2.3.2 Modes of action 2.4 Biosynthesis of silver nanoparticles by Streptomyces 11 2.4.1 Introduction of the genus Streptomyces 11 2.4.2 Green synthesis of silver nanoparticles by Streptomyces 12 2.5 Overview of Crinum latifolium L 14 2.6 Current status of green silver nanoparticles in Vietnam 14 III MATERIALS AND METHODS 15 3.1 Research subjects and materials 15 3.1.1 Location and time of the study 15 3.1.2 Materials .15 3.1.3 Equipment and chemicals 16 iii 3.1.4 Composition of media 16 3.2 Methods 17 3.2.1 Cultivation of Streptomyces spp strains associated with Crinum latifolium L 17 3.2.2 Intracellular silver nanoparticles biosynthesis 17 3.2.3 In vitro antimicrobial activity of synthesized AgNPs 18 3.2.4 Morphological, physiological, and biochemical identification of potent strain 19 3.2.5 Molecular identification based on the 16S rRNA analysis 20 3.2.6 Data analysis .22 IV RESULTS AND DISCUSSION 22 4.1 Antimicrobial screening of silver nanoparticles synthesized by endophytic Streptomyces spp 22 4.1.1 Observation of color change .22 4.1.2 Antimicrobial activity of silver nanoparticles synthesized by Streptomyces sp 23 4.2 Identification of potent Streptomyces spp PCT3 .25 4.2.1 Morphological characteristics of strain PCT3 25 4.2.2 Physiological and biochemical characterization of strain PCT3 26 4.2.3 Molecular identification of strain PCT3 using 16S rRNA analysis 28 4.3 Antimicrobial characterization of PCT3 silver nanoparticles 30 V CONCLUSIONS AND SUGGESTIONS 33 5.1 Conclusions 33 5.2 Suggestions 33 REFERENCES 34 iv LIST OF TABLES Table Antibacterial activity of crude AgNPs synthesized by Streptomyces strains 24 Table Biochemical and physiological characteristics of Streptomyces sp PCT3 27 Table Minimum Inhibitory Concentration of silver nanoparticles produced from S albus PCT3 31 v LIST OF FIGURES Figure 1.1 The shape of AgNPs observed by transmission electron microscopy Figure 1.2 Routes of cytotoxicity action for AgNPs (1) Adhesion to cell wall; (2) Cellular internalization; (3) ROS generation; (4) Genotoxicity 11 Figure 1.3 Mechanism of extracellular and intracellular synthesis of AgNPs by actinomycetes 13 Figure 1.4 The color change observed when cell-free supernatant of the representative strains were treated with mM AgNO3 after 72 h 23 Figure 1.5 Antibacterial activity of crude AgNPs against Candida albicans (A) and Enterococcus faecalis (B) 24 Figure 1.6 The colonial morphology of strain PCT3 observed after days of incubation, at 30°C 26 Figure 1.7 Enzymatic activities of strain PCT3 shown on agar plates containing skim milk (A), starch (B), and CMC (C) 28 Figure 1.8 Agarose gel electrophoresis of the 16S rRNA gene amplicons of Streptomyces sp PCT3 Land M: DNA marker (250 – 10,000 bp) 29 Figure 1.9 Phylogenetic tree based on 16S rRNA gene sequences exhibiting the relationship between Streptomyces spp PCT3 and other closely related type strains 29 Figure 1.10 Zones of inhibition of AgNPs against C albicans ATCC 10231 (A) and P aeruginosa ATCC 9027 (B) 32 vi LIST OF ABBREVIATIONS Abbreviation Full word AgNPs Silver nanoparticles Bio-AgNPs Bio silver nanoparticles CFS Cell-free supernatant CMC Carboxymethyl cellulose MIC Minimum Inhibitory Concentration NADH Nicotinamide Adenine Dinucleotide rDNA Ribosomal DNA ROS Reactive oxygen species SPR Surface plasmon resonance vii ABSTRACT Nanotechnology holds an emerging domain of medical science as it can be utilized virtually in all areas Among metallic nanoparticles, silver nanoparticles (AgNPs) are widely used in biomedical sciences, healthcare, drug–gene delivery, space industries, cosmetics, chemical industries, optoelectronics The applications of AgNPs attribute to their own physical, chemical and biological activities Recently, green approach of AgNPs synthesis is gained attentions due to growing need for developing cost-effective, bio-compatible, and eco-friendly approaches to synthesis AgNPs In this study, endophytic strains from medicinal plant Crinum latifolium L were screened for their ability to synthesize AgNPs with antibacterial property Among them, the AgNPs synthesized by mixing freebiomass filtrate of strain PCT3 with 1 mM AgNO3 were the most promising as indicated by the color intensity and microbial activity Strain PCT3 grew well on ISP2 agar with irregular margin, filamentous, white, umbonate, and rough colonies, which exhibited the typical morphology of Streptomyces Besides, it utilized glucose, fructose, sucrose as carbon sources for growth and produced protease and amylase Phylogenetic analysis of PCT3 based on 16S rRNA gene analysis revealed that PCT3 was closely related to Streptomyces albus Combining morphological, biochemical, and molecular analysis, strain PCT3 was identified as S albus PCT3 Antibacterial characterization of AgNPs from S albus PCT3 revealed that obtained AgNPs were effective against Gram-positive, Gram-negative bacteria with MIC values ranging from 3.9 μg/mL to 31.2 μg/mL In addition, AgNPs strongly inhibited yeast Candida albicans ATCC 10231 In conclusion, the current study is a demonstration of an efficient synthesis of PCT3 by endophytic Streptomyces from C latifolium, which is an interesting subject for development of antimicrobial agents to combat infection viii Figure 1.8 Agarose gel electrophoresis of the 16S rRNA gene amplicons of Streptomyces sp PCT3 Land M: DNA marker (250 – 10,000 bp) The results showed that the 16S rRNA sequence of strain PCT3 showed high similarities to Streptomyces albus NRRL B-1811T (99%) and strain Streptomyces albus NRRC 13015T (99%) This indicated that PCT3 strain might belong to Streptomyces Phylogenetic analysis of PCT3 based on 16S rRNA gene sequences compared to the 16S rRNA gene sequences of hit species highlighted the differential alignment of PCT3 with different species (Figure 4.6) Also, it showed that 16S rRNA sequence of strain PCT3 formed a separate clade with five type strains including S albus NRRL B-1811T, S albus NRRC 13015T, S albus NBRC 13014T, S albus NBRC 15415T, S albus NBRC 13078T Therefore, strain PCT3 was identified as Streptomyces albus PCT3 Figure 1.9 Phylogenetic tree based on 16S rRNA gene sequences exhibiting the relationship between Streptomyces spp PCT3 and other closely related type strains 29 S albus was discovered for the first time by Nagatsu and co-worker in 1962 The S albus strain can be easily isolated from environmental niches such as selfheated compost and soil It could effectively degrade oil cake and straw waste through production of xylanase, which is used for biogas production (B Sathya, 2012) Moreover, S albus was reported to be isolated in grass and active against the cotton aphid Aphis gossypii (Shi et al., 201113) As for secondary metabolites, a number of insecticidal compounds are produced by S albus including flavensomycin, antimycin A, piericidins, macrotetralides, and prasinons (Ruiu et al., 2013) This strain also is preferred host for the heterologous production of versatile secondary metabolites from other bacteria as well as expression of metagenomic DNA clones encoding secondary metabolites Commercial antibiotics such as steffimycin, fredericamycin, isomigrastatin, napyradiomycin, cyclooctatin, thiocoraline, and moenomycin are produced by this strain through the recombinant approach (Kallifidas et al., 2018) Importantly, green synthesis of AgNPs by S albus has not been reported to date, highlighting the novelty of this research 4.3 Antimicrobial characterization of PCT3 silver nanoparticles AgNPs synthesized from free-biomass filtrate of S albus PCT3 was purified and then tested for their own antimicrobial property The results of MIC of purified AgNPs can be seen in Table 4.3 It turned out that AgNPs obtained from free-biomass filtrate were effective against Gram (+) bacteria, Gram (-) bacteria, and yeast Gram-positive bacteria, S aureus ATCC 29213 showed the MIC value of 31.2 μg/mL and E faecalis ATCC 29212 noticed 15.6 μg/mL Among the Gram-negative bacteria, S enterica ATCC 14028 displayed 15.6 μg/mL, E coli ATCC 11105 and P aeruginosa ATCC 9027 noted 3.9 μg/mL It suggested that Gram-negative bacteria are more sensitive to AgNPs than Grampositive bacteria Besides, the MIC value of the AgNPs for C albicans ATCC 10231was determined to be 1.9 µg/mL, which was highest concentration against microbe recorded (Table 4.3) 30 Table 3.Minimum Inhibitory Concentration of silver nanoparticles produced from S albus PCT3 Pathogens MIC (μg/mL) Gram (+) bacteria S aureus ATCC 29213 31.2 E faecalis ATCC 29212 15.6 Gram (-) bacteria S enterica ATCC 14028 15.6 E coli ATCC 11105 3.9 P aeruginosa ATCC 9027 3.9 Yeast C albicans ATCC 10231 1.9 Antimicrobial activity of AgNPs from S albus PCT3 was quite promising Gmelina arborea mediated AgNPs exerted MIC value 90 µg/mL against P aeruginosa and 20 µg/mL of MIC value against E coli Another report proved that the MIC values of AgNPs from S chiangmaiensis SSUT88A against A baumannii, K pneumoniae 1617, P aeruginosa N90PS, and E coli 8564 were 6.8, 27, 13, and 27 µg/mL, respectively (Rosyidah et al., 2022b) They suggested that antibacterial property of AgNPs from PCT3 was higher than those of AgNPs published previously Differently, the MIC value of AgNPs fabricated by Vitis vinifera leaf extract for Candida albicans was 0.331 µg/mL, which was considerably more effective than green AgNPs in this study (ACAY et al., 2019b) Regarding to Staphylococcus aureus, the MIC value was found to be lower than previous works which was reported for Artemisia tournefortiana Rchb extract (12.5 µg/mL), Pleurotus ostreatus (16.1 µg/mL), Desmodium triflorum extracts (27 µg/mL) (Singh & Mijakovic, 2022) 31 Figure 1.10 Zones of inhibition of AgNPs against C albicans ATCC 10231 (A) and P aeruginosa ATCC 9027 (B) Apart from that, agar-well diffusion method further confirmed MIC results All pathogens were sensitive to AgNPs at the concentration ranging from 7.8 – 62.5 µg/mL (Figure 4.7) Of note, Gram-positive bacteria were resistant than Gram-negative bacteria Different to several reports, the antibacterial potential of AgNPs was reported to be more effective against Gram-positive bacteria when compared with Gram-negative bacteria because of their cell wall structure (AlNemrawi et al., 2022) The loss of cell wall integrity and permeability were attributed to the positive charges carried by the AgNPs, which interacted with the negatively charged bacterial cell walls, attached, and entered the bacterial cell So, they suggested an explanation that Gram-positive bacteria are known to have a negative charge on their cell walls due to the presence of teichoic acids linked to either the peptidoglycan or the underlying plasma membrane In contrast, Gram-negative bacteria have an outer layer made of phospholipids and lipopolysaccharides, which reduces the impact of the negative charge in comparison to Gram-positive bacteria The different pattern observed in the AgNPs from S albus PCT3 indicated unknown killing mechanisms against pathogenic bacteria, which remains to be investigated in the future 32 V CONCLUSIONS AND SUGGESTIONS 5.1 Conclusions - In the present study, out of Streptomyces spp from C latifolium showed ability to synthesized AgNPs as indicated by color changes from clear to reddish brown Among them, crude AgNPs synthesized from strain PCT3 showed significant inhibitory effects against pathogens including E faecalis ATCC 29212, C albicans ATCC 10231, E coli ATCC 11105, S epidermidis ATCC 12228, S enterica ATCC 14028, and P aeruginosa ATCC 9027 - Based on morphological and biochemical characteristics, and 16S rRNA gene analysis, the most potent strain was identified as S albus PCT3 - The purified AgNPs synthesized from S albus PCT3 showed remarkable antibacterial activity against Gram-positive and -negative bacteria with MIC values ranging from 3.9 μg/mL to 31.2 μg/mL Of note, C albicans ATCC 10231 was the most sensitive pathogen as indicated by the MIC value of be 1.9 µg/mL 5.2 Suggestions Based on the findings, I offer the following suggestions for further research: - Optimization of cultural and reaction conditions will be required further to improve green synthesis of AgNPs from S albus PCT3 - Spectroscopic and microscopic characterization studies are needed to discover functional groups and the morphological properties of 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