Abstract
Biosynthesis of silver nanoparticles (AgNPs) from marine actinobacteria offers a promising avenue for exploring bacterial extracts as reducing and stabilizing agents. We report extracellular extracts of Rhodococcus rhodochrous (MOSEL-ME29) and Streptomyces sp. (MOSEL-ME28), identified by 16S rRNA gene sequencing for synthesis of AgNPs. Ultrafine silver nanoparticles were biosynthesized using the extracts of R. rhodochrous and Streptomyces sp. and their possible therapeutic applications were studied. The physicochemical properties of nanoparticles were established by HR-SEM/TEM, SAED, UV–Vis, EDS, XRD, and FTIR. UV–Vis spectra displayed characteristic absorption at 430 nm and 412 nm for AgNPs from Streptomyces sp. (S-AgNPs) and Rhodococcus sp. (R-AgNPs), respectively. HR-SEM/TEM, XRD, EDS analysis confirmed the spherical shape, crystalline nature, and elemental formation of silver. Crystallite or grain size was deduced as 5.52 nm for R-AgNPs and 35 nm for S-AgNPs. Zeta-potential indicated electrostatic negative charge for AgNPs, while FTIR revealed the presence of diverse functional groups. Disc diffusion assay indicated the broad-spectrum antibacterial potential of S-AgNPs with the maximum inhibition of B. subtilis while R-AgNPs revealed potency against P. aeruginosa at 10 µg/mL concentration. Biogenic AgNPs revealed antileishmanial activity and the IC50 was calculated as 164 µg/mL and 184 µg/mL for R-AgNPs and S-AgNPs respectively. Similarly, the R-AgNPs and S-AgNPs revealed anti-cancer potential against HepG2 and the IC50 was calculated as 49 µg/mL and 69 µg/mL for R-AgNPs and S-AgNPs, respectively. Moreover, the antioxidant activity showed significant results. MTT assay on RD cells, L20B cells, and Hep-2C indicated intensification in viability by reducing the concentration of R-AgNPs and S-AgNPs. The R-AgNPs and S-AgNPs inhibited sabin-like poliovirus (1TCID50 infection in RD cells). Furthermore, hemocompatibility at low concentrations has been confirmed. Hence, it is concluded that biogenic-AgNPs has the potential to be used in diverse biological applications and that the marine actinobacteria are an excellent resource for fabrication of AgNPs.
Similar content being viewed by others
Data availability
The accession numbers are available in the NCBI genebank as mentioned in the paper in the molecular identification section. Rhodococcus rhodochrous( MOSEL-ME29): MH217573; Streptomyces sp. (MOSEL-ME28): MH217572.
References
Abamor ES (2017) Antileishmanial activities of caffeic acid phenethyl ester loaded PLGA nanoparticles against Leishmania infantum promastigotes and amastigotes in vitro. Asian Pac J Trop Med 10(1):25–34
Abd-Elnaby HM, Abo-Elala GM, Abdel-Raouf UM, Hamed MM (2016) Antibacterial and anticancer activity of extracellular synthesized silver nanoparticles from marine Streptomyces rochei MHM13. Egypt J Aquatic Res 42(3):301–312
Abirami M, Kannabiran K (2016) Streptomyces ghanaensis VITHM1 mediated green synthesis of silver nanoparticles: mechanism and biological applications. Front Chem Sci Eng 10(4):542–551
Acharya D, Singha KM, Pandey P, Mohanta B, Rajkumari J, Singha LP (2018) Shape dependent physical mutilation and lethal effects of silver nanoparticles on bacteria. Sci Rep 8(1):201
Afzal I, Iqrar I, Shinwari ZK, Yasmin A (2017) Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. Plant Growth Regul 81(3):399–408
Ahmad F, Ashraf N, Ashraf T, Zhou R-B, Yin D-C (2019) Biological synthesis of metallic nanoparticles (MNPs) by plants and microbes: their cellular uptake, biocompatibility, and biomedical applications. Appl Microbiol Biotechnol 103(7):2913–2935
Ahmed Mohamed HE, Afridi S, Khalil AT, Zohra T, Ali M, Alam MM, Ikram A, Shinwari ZK, Maaza M (2020) Phyto-fabricated Cr2O3 nanoparticle for multifunctional biomedical applications. Nanomedicine 15(17):1653–1669
Ajitha B, Reddy YAK, Reddy PS (2015) Enhanced antimicrobial activity of silver nanoparticles with controlled particle size by pH variation. Powder Technol 269:110–117
Al-Dhabi N, Mohammed Ghilan A-K, Arasu M (2018) Characterization of silver nanomaterials derived from marine Streptomyces sp. al-dhabi-87 and its in vitro application against multidrug resistant and extended-spectrum beta-lactamase clinical pathogens. Nanomaterials 8(5):279
Al-Dhabi NA, Ghilan A-KM, Esmail GA, Arasu MV, Duraipandiyan V, Ponmurugan K (2019) Environmental friendly synthesis of silver nanomaterials from the promising Streptomyces parvus strain Al-Dhabi-91 recovered from the Saudi Arabian marine regions for antimicrobial and antioxidant properties. J Photochem Photobiol B Biol 197:111529
Ali A, Ambreen S, Javed R, Tabassum S, ul Haq I, Zia M, (2017) ZnO nanostructure fabrication in different solvents transforms physio-chemical, biological and photodegradable properties. Mater Sci Eng, C 74:137–145
Alsammarraie FK, Wang W, Zhou P, Mustapha A, Lin M (2018) Green synthesis of silver nanoparticles using turmeric extracts and investigation of their antibacterial activities. Colloids Surf, B 171:398–405
Asanithi P, Chaiyakun S, Limsuwan P (2012) Growth of silver nanoparticles by DC magnetron sputtering. J Nanomater 2012:79
Baram-Pinto D, Shukla S, Perkas N, Gedanken A, Sarid R (2009) Inhibition of herpes simplex virus type 1 infection by silver nanoparticles capped with mercaptoethane sulfonate. Bioconjug Chem 20(8):1497–1502
Boerma M (2018) Cardiovascular side effects of breast cancer therapy. In: Gender differences in the pathogenesis and management of heart disease. Springer, pp 303–316. https://doi.org/10.1007/978-3-319-71135-5_17
Celebioglu A, Topuz F, Yildiz ZI, Uyar T (2019) One-step green synthesis of antibacterial silver nanoparticles embedded in electrospun cyclodextrin nanofibers. Carbohyd Polym 207:471–479
Chaudhuri SK, Malodia L (2017) Biosynthesis of zinc oxide nanoparticles using leaf extract of Calotropis gigantea: characterization and its evaluation on tree seedling growth in nursery stage. Appl Nanosci 7(8):501–512
Chen N, Zheng Y, Yin J, Li X, Zheng C (2013) Inhibitory effects of silver nanoparticles against adenovirus type 3 in vitro. J Virol Methods 193(2):470–477
Din Fu, Choi JY, Kim DW, Mustapha O, Kim DS, Thapa RK, Ku SK, Youn YS, Oh KT, Yong CS (2017) Irinotecan-encapsulated double-reverse thermosensitive nanocarrier system for rectal administration. Drug Deliv 24(1):502–510
El-Naggar NE-A, Abdelwahed NA (2014) Application of statistical experimental design for optimization of silver nanoparticles biosynthesis by a nanofactory Streptomyces viridochromogenes. J Microbiol 52(1):53–63
Gahlawat G, Choudhury AR (2019) A review on the biosynthesis of metal and metal salt nanoparticles by microbes. RSC Adv 9(23):12944–12967
Gomathi T, Rajeshwari K, Kanchana V, Sudha P, Parthasarathy K (2019) Impact of nanoparticle shape, size, and properties of the sustainable nanocomposites. In: Sustainable polymer composites and nanocomposites. Springer, pp 313–336. https://doi.org/10.1007/978-3-030-05399-4_11
Guntur SR, Kumar NS, Hegde MM, Dirisala VR (2018) In vitro studies of the antimicrobial and free-radical scavenging potentials of silver nanoparticles biosynthesized from the extract of desmostachya bipinnata. Anal Chem Insights 13:1177390118782877
Hadighi R, Mohebali M, Boucher P, Hajjaran H, Khamesipour A, Ouellette M (2006) Unresponsiveness to Glucantime treatment in Iranian cutaneous leishmaniasis due to drug-resistant Leishmania tropica parasites. PLoS Med 3(5):e162
Hameed S, Khalil AT, Ali M, Numan M, Khamlich S, Shinwari ZK, Maaza M (2019) Greener synthesis of ZnO and Ag–ZnO nanoparticles using Silybum marianum for diverse biomedical applications. Nanomedicine 14:6
Hanske C, Sanz-Ortiz MN, Liz-Marzán LM (2018) Silica-coated plasmonic metal nanoparticles in action. Adv Mater 30(27):1707003
Jafri L, Saleem S, Ullah N, Mirza B (2017) In vitro assessment of antioxidant potential and determination of polyphenolic compounds of Hedera nepalensis K. Koch. Arab J Chem 10:S3699–S3706
Javed R, Usman M, Tabassum S, Zia M (2016) Effect of capping agents: structural, optical and biological properties of ZnO nanoparticles. Appl Surf Sci 386:319–326
Karthik L, Kumar G, Kirthi AV, Rahuman A, Rao KB (2014) Streptomyces sp. LK3 mediated synthesis of silver nanoparticles and its biomedical application. Bioprocess Biosyst Eng 37(2):261–267
Khalil AT, Ovais M, Ullah I, Ali M, Shinwari ZK, Hassan D, Maaza M (2018) Sageretia thea (Osbeck) modulated biosynthesis of NiO nanoparticles and their in vitro pharmacognostic, antioxidant and cytotoxic potential. Artif Cells Nanomed Biotechnol 46(4):838–852
Khalil AT, Ovais M, Ullah I, Ali M, Shinwari ZK, Khamlich S, Maaza M (2017a) Sageretia thea (Osbeck) mediated synthesis of zinc oxide nanoparticles and its biological applications. Nanomedicine 12(15):1767–1789
Khalil AT, Ovais M, Ullah I, Ali M, Shinwari ZK, Maaza M (2017b) Physical properties, biological applications and biocompatibility studies on biosynthesized single phase cobalt oxide (Co3O4) nanoparticles via Sageretia thea (Osbeck.). Arab J Chem 13(1): 606–619
Kosmala A, Wright R, Zhang Q, Kirby P (2011) Synthesis of silver nano particles and fabrication of aqueous Ag inks for inkjet printing. Mater Chem Phys 129(3):1075–1080
Kotcherlakota R, Das S, Patra CR (2019) Therapeutic applications of green-synthesized silver nanoparticles. In: Green synthesis, characterization and applications of nanoparticles. Elsevier, pp 389–428. https://doi.org/10.1016/B978-0-08-102579-6.00017-4
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
Kumar V, Choudhary AK, Kumar P, Sharma S (2019) Nanotechnology: nanomedicine, nanotoxicity and future challenges. Nanosci Nanotechnol Asia 9(1):64–78
Lin X, Huang Y, Fang M, Wang J, Zheng Z, Su W (2005) Cytotoxic and antimicrobial metabolites from marine lignicolous fungi Diaporthe Sp. FEMS Microbiol Lett 251(1):53–58
Malagoli D (2007) A full-length protocol to test hemolytic activity of palytoxin on human erythrocytes. Invertebr Surviv J 4(2):92–94
Manimaran M, Kannabiran K (2017) Actinomycetes-mediated biogenic synthesis of metal and metal oxide nanoparticles: progress and challenges. Lett Appl Microbiol 64(6):401–408
Manivasagan P, Venkatesan J, Sivakumar K, Kim S-K (2016) Actinobacteria mediated synthesis of nanoparticles and their biological properties: a review. Crit Rev Microbiol 42(2):209–221
Mohamed HEA, Afridi S, Khalil AT, Ali M, Zohra T, Akhtar R, Ikram A, Shinwari ZK, Maaza M (2020a) Promising antiviral, antimicrobial and therapeutic properties of green nanoceria. Nanomedicine 15(05):467–488
Mohamed HEA, Afridi S, Khalil AT, Ali M, Zohra T, Alam MM, Ikram A, Shinwari ZK, Maaza M (2019) Phytosynthesis of BiVO4 nanorods using Hyphaene thebaica for diverse biomedical applications. AMB Express 9(1):1–14
Mohamed HEA, Afridi S, Khalil AT, Ali M, Zohra T, Salman M, Ikram A, Shinwari ZK, Maaza M (2020b) Bio-redox potential of Hyphaene thebaica in bio-fabrication of ultrafine maghemite phase iron oxide nanoparticles (Fe2O3 NPs) for therapeutic applications. Mater Sci Eng C 112:110890
Ninganagouda S, Rathod V, Singh D, Hiremath J, Singh AK, Mathew J (2014) Growth kinetics and mechanistic action of reactive oxygen species released by silver nanoparticles from Aspergillus niger on Escherichia coli. BioMed Res Int. https://doi.org/10.1155/2014/753419
Ovais M, Ahmad I, Khalil AT, Mukherjee S, Javed R, Ayaz M, Raza A, Shinwari ZK (2018a) Wound healing applications of biogenic colloidal silver and gold nanoparticles: recent trends and future prospects. Appl Microbiol Biotechnol 2018:1–14
Ovais M, Khalil A, Ayaz M, Ahmad I, Nethi S, Mukherjee S (2018b) Biosynthesis of metal nanoparticles via microbial enzymes: a mechanistic approach. Int J Mol Sci 19(12):4100
Ovais M, Khalil AT, Islam NU, Ahmad I, Ayaz M, Saravanan M, Shinwari ZK, Mukherjee S (2018c) Role of plant phytochemicals and microbial enzymes in biosynthesis of metallic nanoparticles. Appl Microbiol Biotechnol 102(16):6799–6814
Ovais M, Zia N, Ahmad I, Khalil AT, Raza A, Ayaz M, Sadiq A, Ullah F, Shinwari ZK (2018d) Phyto-therapeutic and nanomedicinal approaches to cure Alzheimer’s disease: present status and future opportunities. Front Aging Neurosci 2018:10
Patil MP, Kim G-D (2018) Marine microorganisms for synthesis of metallic nanoparticles and their biomedical applications. Colloids Surf, B 172:487–495
Patil YM, Rajpathak SN, Deobagkar DD (2019) Characterization and DNA methylation modulatory activity of gold nanoparticles synthesized by Pseudoalteromonas strain. J Biosci 44(1):15
Pugazhenthiran N, Anandan S, Kathiravan G, Prakash NKU, Crawford S, Ashokkumar M (2009) Microbial synthesis of silver nanoparticles by Bacillus sp. J Nanopart Res 11(7):1811
Racaniello VR (1996) Early events in poliovirus infection: virus-receptor interactions. Proc Natl Acad Sci 93(21):11378–11381
Rahman S, Rahman L, Khalil AT, Ali N, Zia D, Ali M, Shinwari ZK (2019) Endophyte-mediated synthesis of silver nanoparticles and their biological applications. Appl Microbiol Biotechnol 2019:1–19
Romanova LI, Belov GA, Lidsky PV, Tolskaya EA, Kolesnikova MS, Evstafieva AG, Vartapetian AB, Egger D, Bienz K, Agol VI (2005) Variability in apoptotic response to poliovirus infection. Virology 331(2):292–306
Saravanan M, Barik SK, MubarakAli D, Prakash P, Pugazhendhi A (2018) Synthesis of silver nanoparticles from Bacillus brevis (NCIM 2533) and their antibacterial activity against pathogenic bacteria. Microb Pathog 116:221–226
Shah A, Lutfullah G, Ahmad K, Khalil AT, Maaza M (2018) Daphne mucronata-mediated phytosynthesis of silver nanoparticles and their novel biological applications, compatibility and toxicity studies. Green Chem Lett Rev 11(3):318–333
Shanmuganathan R, MubarakAli D, Prabakar D, Muthukumar H, Thajuddin N, Kumar SS, Pugazhendhi A (2018) An enhancement of antimicrobial efficacy of biogenic and ceftriaxone-conjugated silver nanoparticles: green approach. Environ Sci Pollut Res 25(11):10362–10370
Shanthi S, Jayaseelan BD, Velusamy P, Vijayakumar S, Chih CT, Vaseeharan B (2016) Biosynthesis of silver nanoparticles using a probiotic Bacillus licheniformis Dahb1 and their antibiofilm activity and toxicity effects in Ceriodaphnia cornuta. Microb Pathog 93:70–77
Sharma A, Goyal AK, Rath G (2018) Recent advances in metal nanoparticles in cancer therapy. J Drug Target 26(8):617–632
Singh H, Du J, Singh P, Yi TH (2018) Extracellular synthesis of silver nanoparticles by Pseudomonas sp. THG-LS1 4 and their antimicrobial application. J Pharm Anal 8(4):258–264
Singh R, Shedbalkar UU, Wadhwani SA, Chopade BA (2015) Bacteriagenic silver nanoparticles: synthesis, mechanism, and applications. Appl Microbiol Biotechnol 99(11):4579–4593
Singh R, Wagh P, Wadhwani S, Gaidhani S, Kumbhar A, Bellare J, Chopade BA (2013) Synthesis, optimization, and characterization of silver nanoparticles from Acinetobacter calcoaceticus and their enhanced antibacterial activity when combined with antibiotics. Int J Nanomed 8:4277
Sinha SN, Paul D, Halder N, Sengupta D, Patra SK (2015) Green synthesis of silver nanoparticles using fresh water green alga Pithophora oedogonia (Mont.) Wittrock and evaluation of their antibacterial activity. Appl Nanosci 5(6):703–709
Sivasankar P, Seedevi P, Poongodi S, Sivakumar M, Murugan T, Sivakumar L, Sivakumar K, Balasubramanian T (2018) Characterization, antimicrobial and antioxidant property of exopolysaccharide mediated silver nanoparticles synthesized by Streptomyces violaceus MM72. Carbohyd Polym 181:752–759
Sosa IO, Noguez C, Barrera RG (2003) Optical properties of metal nanoparticles with arbitrary shapes. J Phys Chem B 107(26):6269–6275
Subbaiya R, Saravanan M, Priya AR, Shankar KR, Selvam M, Ovais M, Balajee R, Barabadi H (2017) Biomimetic synthesis of silver nanoparticles from Streptomyces atrovirens and their potential anticancer activity against human breast cancer cells. IET Nanobiotechnol 11(8):965–972
Sujitha V, Murugan K, Paulpandi M, Panneerselvam C, Suresh U, Roni M, Nicoletti M, Higuchi A, Madhiyazhagan P, Subramaniam J (2015) Green-synthesized silver nanoparticles as a novel control tool against dengue virus (DEN-2) and its primary vector Aedes aegypti. Parasitol Res 114(9):3315–3325
Sukanya M, Saju K, Praseetha P, Sakthivel G (2013) Therapeutic potential of biologically reduced silver nanoparticles from actinomycete cultures. J Nanosci 2013:1–18
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 101(30):11030–11035
Tan Y-W, Ge G-H, Zhao W, Gan J-H, Zhao Y, Niu Z-L, Zhang D-J, Chen L, Yu X-J, Yang L-J (2012) YMDD motif mutations in chronic hepatitis B antiviral treatment naïve patients: a multi-center study. Braz J Infect Dis 16(3):250–255
Tanveer F, Shehroz M, Ali M, Xie Y, Abbasi R, Shinwari ZK, Yasmin A (2021) Genome sequence analysis and bioactivity profiling of marine-derived actinobacteria, Brevibacterium luteolum, and Cellulosimicrobium funkei. Arch Microbiol 2021:1–10
Thomas R, Jasim B, Mathew J, Radhakrishnan E (2012) Extracellular synthesis of silver nanoparticles by endophytic Bordetella sp. isolated from Piper nigrum and its antibacterial activity analysis. Nano Biomed Eng 4(4):183–187
Thuy NT, Huy TQ, Nga PT, Morita K, Dunia I, Benedetti L (2013) A new nidovirus (NamDinh virus NDiV): Its ultrastructural characterization in the C6/36 mosquito cell line. Virology 444(1–2):337–342
Tien D-C, Tseng K-H, Liao C-Y, Huang J-C, Tsung T-T (2008) Discovery of ionic silver in silver nanoparticle suspension fabricated by arc discharge method. J Alloy Compd 463(1–2):408–411
Tran QH, Le A-T (2013) Silver nanoparticles: synthesis, properties, toxicology, applications and perspectives. Adv Nat Sci Nanosci Nanotechnol 4(3):033001
Xiang D-x, Chen Q, Pang L, Zheng C-l (2011) Inhibitory effects of silver nanoparticles on H1N1 influenza A virus in vitro. J Virol Methods 178(1–2):137–142
Xu Q, Ke X, Cai D, Zhang Y, Fu F, Endo T, Liu X (2018) Silver-based, single-sided antibacterial cotton fabrics with improved durability via an l-cysteine binding effect. Cellulose 25(3):2129–2141
Zayed MF, Eisa WH, Shabaka A (2012) Malva parviflora extract assisted green synthesis of silver nanoparticles. Spectrochim Acta Part A Mol Biomol Spectrosc 98:423–428
Acknowledgements
The authors are thankful for the assistance provided by the National Institute of Health-Pakistan, UNESCO UNISA Chair in Nanosciences and Nanotechnology-South Africa, University of Western Cape-South Africa, and Pakistan Academy of Sciences, Islamabad.
Funding
No funding was received for conducting this research.
Author information
Authors and Affiliations
Contributions
Alam A and Tanveer F contributed equally in experimentation, data analysis, interpretation, and manuscript preparation. Khalil AT contributed to the physical characterization of nanoparticles, data interpretation, and overall manuscript review. Maaza M and Khamlich S facilitated the experimentation and analysis of structural techniques employed. Shinwari ZK and Ali M supervised the research and provided critical analysis of the written manuscript. Zohra T performed the antiviral assay and interpreted the results. Alam MM, Salman M, and Ikram A provided the facility for the antiviral assay and oversaw the antiviral data analysis and interpretation.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Alam, A., Tanveer, F., Khalil, A.T. et al. Silver nanoparticles biosynthesized from secondary metabolite producing marine actinobacteria and evaluation of their biomedical potential. Antonie van Leeuwenhoek 114, 1497–1516 (2021). https://doi.org/10.1007/s10482-021-01616-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-021-01616-5