Appl Microbiol Biotechnol DOI 10.1007/s00253-016-7300-7

MINI-REVIEW

Biogenic selenium nanoparticles: current status and future prospects Sweety A. Wadhwani 1 & Utkarsha U. Shedbalkar 1,2 & Richa Singh 1 & Balu A. Chopade 1,3

Received: 4 September 2015 / Revised: 30 December 2015 / Accepted: 5 January 2016 # Springer-Verlag Berlin Heidelberg 2016

Abstract Selenium nanoparticles (SeNPs) are gaining importance in the field of medicine owing to their antibacterial and anticancer properties. SeNPs are biocompatible and non-toxic compared to the counterparts, selenite (SeO3−2) and selenate (SeO4−2). They can be synthesized by physical, chemical, and biological methods and have distinct bright orange-red color. Biogenic SeNPs are stable and do not aggregate owing to natural coating of the biomolecules. Various hypotheses have been proposed to describe the mechanism of microbial synthesis of SeNPs. It is primarily a two-step reduction process from SeO4−2 to SeO3−2 to insoluble elemental selenium (Se0) catalyzed by selenate and selenite reductases. Phenazine-1carboxylic acid and glutathione are involved in selenite reduction. Se factor A (SefA) and metalloid reductase Rar A present on the surface of SeNPs confer stability to the nanoparticles. SeNPs act as potent chemopreventive and chemotherapeutic agents. Conjugation with antibiotics enhances their anticancer efficacy. These also have applications in nanobiosensors and environmental remediation.

Keywords Selenium nanoparticles . Selenate reduction . Mechanism . Antibacterial activity . Anticancer

* Balu A. Chopade [email protected]

1

Department of Microbiology, Savitribai Phule Pune University, Pune, Maharashtra 411007, India

2

Department of Biochemistry, The Institute of Science, Mumbai, Maharashtra 400032, India

3

Dr. Babasaheb Ambedkar Marathwada University, Aurangabad, Maharashtra 431004, India

Introduction Selenium (Se) is an essential element in human and animal body in low concentration. It is a necessary dietary constituent of at least 25 human selenoproteins and enzymes containing selenocysteine (Zhang and Spallholz 2011). In the environment, it exists in many oxidation states (−2, 0, +4, +6) and forms, such as ionic selenite (Na 2 SeO 3 ) and selenate (Na2SeO4), solid state Se (0), selenomethionine (SeMet)/ selenocysteine, etc. (Bo li et al. 2014; Biswas et al. 2011). Selenite is the most toxic form of Se; hence, biogeochemical cycles involving reduction of selenite (Se+4) to elemental selenium (Se0) are of paramount importance (Jayaweera and Biggar 1996). Selenium nanoparticles (SeNPs) are gaining importance in electronics and optics due to their enhanced semiconducting, photoconducting, photoelectrical, and catalytic properties (Barnaby et al. 2011; Srivastava and Mukhopadhyay 2013; Zhang and Spallholz 2011). SeNPs exhibit low cytotoxicity compared to selenium (Se) compounds and posses excellent anticancer and therapeutic activities making them apt for medicinal applications (Barnaby et al. 2011; Forootanfara et al. 2013; Peng et al. 2007; Shakibaie et al. 2010; Wang et al. 2007). Se is required as a cofactor for glutathione peroxidases and thioredoxin reductases in animals, which is supplied in their meal as an essential element. However, studies have shown that SeNPs are utilized more efficiently than inorganic and organic selenium (Benko et al. 2012; Hu et al. 2012; Shi et al. 2011; Zhang and Spallholz 2011). SeNPs can be synthesized through physical methods, such as laser ablation, UV radiation, and hydrothermal techniques (Iranifam et al. 2013; Overschelde et al. 2013; Quintana et al. 2002). Chemical synthesis is mediated by precipitation, acid decomposition, and catalytic reduction using ascorbic acid, glucose, sulfur dioxide, sodium dodecyl sulfate, etc.

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(Dwivedi et al. 2011; Hong Lin et al. 2004; Zhang et al. 2010). However, these methods require high temperature, acidic pH, and harsh chemicals (Iranifam et al. 2013), which may render the nanoparticles unsafe for biomedical applications. Biosynthesis of SeNPs is safe and inexpensive, and employ eco-friendly non-toxic materials (Ghosh et al. 2012a; b; Singh et al. 2013; Singh et al. 2015; Salunke et al. 2014; Shedbalkar et al. 2014; Wadhwani et al. 2014). Further, biogenic SeNPs are stable due to natural coating of the organic molecules and do not aggregate with time, whereas external addition of stabilizing agents is required in chemical synthesis (Nancharaiah and Lens 2015a). Despite the advances in the research of biological SeNPs, there is no review compiling this information. This mini review focuses mainly on biogenic synthesis of SeNPs, its mechanism, and applications in various fields. Biogenic synthesis of SeNPs Biogenic synthesis of SeNPs is mediated by bacteria, fungi, and plants as enlisted in Table 1. Synthesis by bacteria Many bacteria are known to exhibit Se resistance (Deshpande et al. 1993) and synthesize SeNPs as one of the mechanisms of Se detoxification (Kessi et al. 1999). Synthesis of these nanoparticles can be extracellular, intracellular, or membrane bound (Table 1). Gerrard and colleagues firstly observed Se deposits on the cell wall and cell membrane of Escherichia coli under electron microscopy. It has been suggested that the bacterial cells have the ability to reduce sodium selenite present in the culture medium to elemental Se (Gerrard et al. 1974). After that, many Gram-negative and Gram-positive bacteria have been reported to reduce selenate and selenite (Table 1). Veillonella atypica and Pseudomonas sp. RB synthesize quantum dots, such as CdSe and ZnSe (Ayano et al. 2014; Pearce et al. 2008). There are also two reports on SeNP synthesis by Actinomycetes (Ahmad et al. 2015; Forootanfara et al. 2014).

colored colonies on Czapek-Dox agar containing sodium selenate (Gharieb et al. 1995). Synthesis by plants In spite of the fact that a large number of plants are reported for nanoparticle synthesis (Ghosh et al. 2012a; b; Mittal et al. 2013; Salunke et al. 2014), there are only five reports on phytogenic synthesis of SeNPs (Chen et al. 2008; Prasad et al. 2012; Prasad et al. 2013; Ramamurthy et al. 2013; Li et al. 2007). Leaf extract of Capsicum annuum reduces SeO3−2 to red color indicating formation of SeNPs (Li et al. 2007). Dried fruit extract of Vitis vinifera can synthesize spherical SeNPs in the range of 3–18 nm (Sharma et al. 2014). Polysaccharides extracted from Undaria pinnatifida, edible seaweed, enhance the stability of SeNPs (Chen et al. 2008). By definition, particles having one dimension up to 100 nm should be called as nanoparticles (Shedbalkar et al. 2014; Singh et al. 2015). However, it is important to note that Se sub-micronic particles of size more than 100 nm are also reported as SeNPs in the literature. Duganella sp. and Agrobacterium sp. reduce selenite to elemental Se of size 140–200 and 185–190 nm, respectively (Bajaj et al. 2012). There are only few reports on biogenic Se particles in the range of 1–100 nm (Dwivedi et al. 2013; Prasad et al. 2013; Prasad and Selvaraj 2014; Sharma et al. 2014; Tam et al. 2010). However, size of particles can be controlled by optimizing the physicochemical parameters during synthesis. Such studies are reported from our laboratory in case of silver, gold, and platinum nanoparticles using bacteria and plants (Gaidhani et al. 2014; Gaidhani et al. 2013; Ghosh et al. 2012b; Singh et al. 2013; Wadhwani et al. 2014). Like all nanomaterials, morphological, compositional, and spectroscopic characterizations of biogenic SeNPs are carried out using microscopy (Fig. 1), spectroscopy, diffraction, light scattering, and nanoparticle tracking analysis (Ghosh et al. 2015; Husen and Siddiqi 2014; Kitture et al. 2015; Shedbalkar et al. 2014; Wadhwani et al. 2014). Mechanism of microbial synthesis of SeNPs

Synthesis by fungi Till date, only five reports have described fungal mediated synthesis of SeNPs (Gharieb et al. 1995; Sarkar et al. 2011; Vetchinkina et al. 2013; Zare et al. 2012). Extracellular production of monodispersed spherical SeNPs has been reported in Aspergillus terreus isolated from soil and Alternaria alternate isolated from leaf spot on Stevia rebaudiana. Edible Lentinula edodes synthesize SeNPs intracellularly (Sarkar et al. 2011; Vetchinkina et al. 2013; Zare et al. 2012). Fusarium sp. and Trichoderma reesei show red-

Thauera selenatis, Enterobacter cloacae SLD1a-1, and E. coli have been extensively studied for selenate reduction (Butler et al. 2012; Kessi 2006; Ridley et al. 2006; Schröder et al. 1997; Yee et al. 2007), which led researchers to elucidate the mechanism behind the formation of SeNPs in bacteria (Fig. 2). Bacteria utilize selenate and convert it into red allotropes of Se0 that are usually observed as SeNPs accumulated in the cell or in the culture medium (Butler et al. 2012). Primarily, selenate reduction is a two-step reduction process: (i) selenate (SeO4−2) to selenite (SeO3−2) catalyzed by selenate reductases

Spherical – – Spherical – –

150* 140–200*

100 – – 100 – –

– Soil Soil MTCC, IMTECH, Chandigarh – Drainage slough in Nevada Dead sea Geomicrobiology laboratory (University of Manchester) collection – Laboratory bioreactor Environment Fresh water sample ATCC –

Thauera selenatis Duganella sp.

Agrobacterium sp. Zooglea ramigera Rhodospirillum rubrum Sulfurospirillum barnesii Selenihalanaerobacter shriftii

Geobacter sulfurreducens

80–220* 150–200* 50–400* -

Fresh sea water Coalmine soil Anhui Institute Soil

–

–

Spherical Spherical Spherical –

Spherical

Spherical

≤270*

220*

– –

–

Spherical

Spherical Spherical Spherical Spherical Spherical

Spherical Spherical

Spherical Spherical Spherical

–

40–700*

UTEX

Pond sediment Soil –

Stenotrophomonas maltophilia Stenotrophomonas maltophilia Salmonella enteric

Synechococcus leopoliensis Gram positive bacteria Bacillus sp. MSh-1 Bacillus cereus Bacillus subtilis Bacillus subtilis

Soil Rhizosphere soil

Pseudomonas fluorescens

Stenotrophomonas maltophilia

Shewanella oneidensis MR-1 Rhizobium sp. strain B1 Moraxella bovis Enterobacter cloacae SLD1a-1 Enterobacter cloacae SLD1a-1 Pseudomonas stutzeri

50–500* 24–122* 11–20

Other institute DSMZ Laboratory culture collection

Pseudomonas alcaliphila E. coli K-12 Shewanella sp.

185–190* 30–150* – 300* 300*

90–320* 30–150* 30–300*

Spherical Spherical Spherical

140*

Wheat rhizosphere

Spherical

Shape

– Industrial waste impacted soil River

Gram negative bacteria Pseudomonas aeruginosa

Size (nm)

Klebsiella pneumonia Microbacterium sp. ARB05 Pantoea agglomerans

Source of isolation

Microorganisms and plants reported for synthesis of SeNPs

Microorganisms

Table 1

Intracellular Intracellular and cell bound Extracellular

On cell surface

Intracellular and extracellular Near periphery of cell wall

Intracellular – Intracellular Near cell surface Periplasmic membrane Cell bound and extracellular Intracellular

Extracellular Extracellular Intracellular Extracellular Extracellular

Intracellular Extracellular and cell bound

Intracellular Extracellular Intracellular

Intracellular Extracellular Intracellular

Extracellular

Location

Shakibaie et al. 2010 Dhanjal and Cameotra 2010 Wang et al. 2010 Garbisu et al. 1996

Hnain et al. 2013

Dungan et al. 2003 Lampis et al. 2012 Guymer et al. 2009

Gregorio et al. 2005

Garbisu et al. 1996

Bo li et al. 2014 Hunter and Kuykendall 2007 Biswas et al. 2011 Losi and Frankenberger 1997 Watts et al. 2003 Lortie et al. 1992

Fellowes et al. 2011

Bajaj et al. 2012 Srivastava and Mukhopadhyay 2013 Kessi et al. 1999 Oremland et al. 2004 Oremland et al. 2004

Debieux et al. 2011 Bajaj et al. 2012

Zhang et al. 2011 Dobias and Suvorova 2011 Tam et al. 2010

Kazempour et al. 2013 Prasad et al. 2012 Torres et al. 2012

Dwivedi et al. 2013

References

Appl Microbiol Biotechnol

50–150* 200–500* 60–80 10–80 3–18

– – – – –

28–123* 17

Soil Insect

Spherical

Polydispersed

Spherical Polygonal

Rods

–

Fruit extract

Seed extract Leaves extract Leaves extract Leaf extract

–

On the surfaces of hyphae and conidia

Sharma et al. 2014

Ramamurthy et al. 2013 Li et al. 2007 Prasad et al. 2013 Prasad and Selvaraj 2014

Ahmad et al. 2015

Forootanfara et al. 2014

Gharieb et al. 1995

Gharieb et al. 1995

Hariharan et al. 2012 Zare et al. 2012 Sarkar et al. 2011

*Size ≥100 nm but reported as nanoparticles

ATCC American Type Culture Collection, MTCC Microbial Type Culture Collection, DSMZ Deutsche Sammlung von Mikroorganismen und Zellkulturen culture collection, UTEX University Of Texas Culture Collection Of Algae

– Not reported

Vitis vinifera

Streptomyces bikiniensis Plants Trigonella foenum-graecum (fenugreek) Capsicum annuum Lemon Terminalia arjuna

Actinomycetes Streptomyces microflavus

–

–

– –

–

Fusarium sp.

Trichoderma reeii

Extracellular Extracellular Extracellular

– Spherical Spherical

MTCC Chandigarh Soil Leaf spot on Stevia rebaudiana –

30–100 47 30–150*

Lampis et al. 2014 Oremland et al. 2004

Between the cell wall and the plasma membrane. Extracellular Extracellular

Domokos-Szabolcsy et al. 2012 Yazdi et al. 2013

References

Location

Intracellular Intracellular

– >250*

– Persian-type culture collection

Spherical Spherical

Shape

Spherical –

50–400* 300*

Size (nm)

Soil Mono Lake in California

Source of isolation

Saccharomyces cerevisiae Aspergillus terreus Alternaria alternate

Lactobacillus acidophilus Lactobacillus plantarum Fungi

Bacillus mycoides Bacillus selenitireducens

Microorganisms

Table 1 (continued)

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Appl Microbiol Biotechnol Fig. 1 Electron micrographs of SeNPs synthesized by microorganisms and plants. TEM image of a intracellular SeNPs synthesized by T. selenatis (Butler et al. 2012), b extracellular SeNPs by B. selenitreducens (Oremland et al. 2004), c SeNPs synthesized by Bacillus sp. MSh-1 a (Shakibaie et al. 2010), d SeNPs synthesized by hyphae of Lentinula edodes (Vetchinkina et al. 2013), e SeNPs synthesized by Terminalia arjuna leaf extract (Prasad and Selvaraj 2014), f ESEM micrographs of SeNPs on B. cereus cell surface (Dhanjal and Cameotra 2010), g FESEM micrograph of SeNPs synthesized by Capsicum annuum L (Li et al. 2007). SEM image of SeNPs synthesized by h Duganella (Bajaj et al. 2012), i Culture supernatant of A. terrus BZ1 (Zare et al. 2012)

a

b

c

d

e

f

g

h

i

and (ii) selenite to insoluble elemental selenium (Se0) catalyzed by nonspecific selenite reductases, which predominantly include nitrite and sulphite reductases (Kessi and Hanselmann 2004; Ridley et al. 2006). Such reductions are Fig. 2 Schematic diagrams showing the proposed mechanisms for reduction of selenate/selenite by microorganisms. a Selenite reduction and anaerobic respiration in S. oneidensis MR-1 (Bo li et al. 2014), b Reduction of selenite in R. rubrum and E. coli by glutathione (GSH) (Kessi and Hanselmann 2004)

observed under aerobic, anoxic, and anaerobic conditions (Butler et al. 2012; Debieux et al. 2011; Kessi et al. 1999; Losi and Frankenberger 1997; Nancharaiah and Lens 2015b; Watts et al. 2003).

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Selenate reductase Selenate reductase is the key enzyme for the reduction of selenate and exists in soluble and membranous forms in many bacteria (B bien et al. 2002; Butler et al. 2012; Ridley et al. 2006; Watts et al. 2003; Yee et al. 2007). Periplasmic selenate reductase (Ser) is encoded by the SerABCD operon (Butler et al. 2012; Debieux et al. 2011; Krafft et al. 2000). It is a trimeric molybdenum-containing enzyme consisting of a catalytic subunit (SerA), a Fe-S protein (SerB), and a heme b protein (SerC). Membrane-bound selenate reductase is secreted from the cytoplasm through the twin-arginine translocation (TAT) translocase apparatus (Ma et al. 2009) and is embedded in the inner cell membrane (Watts et al. 2003). Alike soluble form, it is also a trimeric complex with an active subunit of 100 kDa oriented towards the periplasmic compartment (Butler et al. 2012). Oxygen sensing protein encoded by global anaerobic regulatory gene fnr (fumarate nitrate reduction regulator) regulates the expression of selenate reductase under suboxic conditions in E. cloacae SLD1a-1 (Yee et al. 2007). Ser reduces selenate to selenite by accepting electrons from the periplasmic c-type cytochromes involving both QCR (quinol-cytochrome C oxidoreductase) and QDH (quinol dehydrogenase). Membranous selenate reductase is in direct association with cytoplasmic membranes and involves electron transfer from Q-pool through one of the core subunits (Butler et al. 2012). The enzyme acts in both aerobic and anaerobic conditions. Menaquinone, a small lipid-soluble molecule, is synthesized and functions as an electron carrier under anaerobic conditions in bacteria. It has been shown to play the role of electro donor for selenate reductase in E. cloacae SLDa1 (Ma et al. 2009). Molybdenum acts as an activator of selenate reductase while tungsten inhibits the enzyme activity (Watts et al. 2003). Selenite reductases Selenite is released in the periplasm after reduction. Bacteria cannot utilize selenite as the sole electron acceptor and it is further reduced to elemental selenium by periplasmic nonspecific selenite reductases. These reductases include various enzyme systems, such as nitrite reductase, sulfite reductase, and glutathione reductase (Butler et al. 2012), and depending up on bacterial species, they may interact or act independently. For example, in Rhodobacter capsulatus and Rhodospirillum rubrum, selenite metabolism is constitutively expressed (Kessi and Hanselmann 2004; Kessi 2006). There is a strong interaction between nitrite reduction and selenite reduction pathways in R. capsulatus, but these pathways operate independently in R. rubrum (Kessi and Hanselmann 2004; Kessi 2006). In Shewanella oneidensis, a dissimilatory metal-reducing bacterium, anaerobic respiration and selenite reduction occur

simultaneously (Bo li et al. 2014). Fumarate reductase present in its periplasm is responsible for selenite reduction, which receives continuous supply of electrons from NADH dehydrogenase and the quinol pool through cytochrome C (Fig. 2a) Besides this, phenazine-1-carboxylic acid, NADH, NADH-dependent reductases, and disulfide reductase are suggested to play significant roles in selenite reduction (Dwivedi et al. 2013; Garbisu et al. 1995). TAT translocase apparatus and TorD-like chaperone are essential for complete reduction of selenate to elemental Se in enteric bacteria like Salmonella enterica and E. coli (Guymer et al. 2009) as shown in Fig. 2a. Selenite can also be reduced to Se0 in abiotic reactions with reduced thiols like glutathione. It converts selenite to selenodiglutathione (GS-Se-SG) by donating electrons. Selenodiglutathione is further reduced by glutathione reductase (GR) or thioredoxin reductase (TR) leading to the formation of selenopersulfide of glutathione, which dismutates into reduced glutathione and elemental Se (Kessi and Hanselmann 2004; Kessi 2006) as depicted in Fig. 2b. Induction of thioredoxin and TR in Bacillus subtilis has been speculated to be involved in reduction of selenite to SeNPs (Garbisu et al. 1995; Garbisu et al. 1999; Swerdlow and Setlow 1983). Post reduction, SeNPs accumulate in the bacterial cell during mid- to late exponential growth phases and are secreted into the surrounding medium in a stationary phase (Butler et al. 2012). Proteins have been suggested to play an important role in the assembly of nanospheres (Kaur et al. 2009). Selenium factor A (Sef A), a protein of ~94.5 kDa, has been shown to accompany SeNPs during their export from the cytoplasmic compartment. This protein helps in biomineralization and stabilization of the nanoparticles (Butler et al. 2012). Of the known SeNPs binding proteins, metalloid reductase Rar A has the highest number of peptides with strong affinity for SeNPs conferring stability to them (Lenz et al. 2011). Propanol-preferring alcohol dehydrogenase (AdhP) protein controls the size distribution of SeNPs, where a threefold decrease in size of SeNPs has been observe in its presence (Dobias and Suvorova 2011). Bovine serum albumin affects the shape of SeNPs (Kaur et al. 2009). The concentration ratio of bovine serum albumin to Na2SeO3 controls the synthesis of crystalline Se nanobars (6:1) and amorphous nanospheres (1:1) (Kaur et al. 2009). Proteins containing tyrosine, tryptophan, and/or phenylalanine residues play an important role in SeNP synthesis (Li et al. 2007). Phytochemicals such as alkaloids, flavonoids, amino acids, proteins, carbohydrates, cardiac glycosides, and saponins present in leaf or seed extract are responsible for selenate reduction (Li et al. 2007; Prasad and Selvaraj 2014; Ramamurthy et al. 2013).

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Applications of SeNPs SeNPs have wide applications in medicine, therapeutics, biosensors, and environmental remediation (Fig. 3). This section is mainly intended to describe the applications of biogenic SeNPs. Medicine SeNPs have found applications in medicine as antimicrobial, antioxidant, and anticancer agents (Forootanfara et al. 2013; Hariharan et al. 2012; Torres et al. 2012; Yang et al. 2012; Yazdi et al. 2012). Antimicrobial activity SeNPs synthesized from a biological source possess a significant antimicrobial activity against pathogenic bacteria, fungi, and yeast. These exhibit concentration- and size-dependent effects against the tested microorganisms (Hariharan et al. 2012), unlike the study of Singh et al. reporting higher antibacterial action of silver nanoparticles against Gram-negative bacteria (Singh et al. 2013). SeNPs can inhibit both Gramnegative and Gram-positive bacteria with equal efficacy (Hariharan et al. 2012). Further, SeNPs have the ability to disrupt microbial biofilms (Zonaro et al. 2015). SeNPs also exhibit antifungal activity by inhibiting spore germination. These are reported to inhibit dermatophytes like Malassezia

sympodialis and Malassezia furfur (Shahverdi et al. 2010). However, unlike antibiotics, SeNPs did not show a post antibiotic effect (PAE), which is defined as the potential of a substance to delay regrowth of a microbial population after short-term exposure and removal of an antimicrobial compound. In a contradictory study, pre-exposure to SeNPs has been shown to decrease the lag phase of fungus, Aspergillus niger, thereby promoting its growth (Kazempour et al. 2013). This might be due to the ability of A. niger to utilize Se from nanoparticles as a trace element. SeNPs can serve as potential therapeutic agents against cutaneous and visceral leishmaniasis as these are reported to kill promastigotes and amastigotes of Leishmania infantum and Leishmania major with IC50 values ranging from 1 to 25 μg/ml (Beheshti et al. 2013; Soflaei et al. 2012). Moreover, SeNPs are biocompatible with uninfected macrophages (Soflaei et al. 2012) and cure the localized lesions of cutaneous leishmaniasis in 14 days in mice (Beheshti et al. 2013). Biogenic SeNPs also exhibit a potent scolicidal activity against Echinococcus granulosus, a parasitic platyhelminth causing cystic hydatid disease (Mahmoudvand et al. 2014). Antioxidant activity SeNPs scavenge reactive oxygen species (ROS), such as 1,1diphenyl-2-picrylhydrazyl (DPPH), superoxide anion (O2•_), singlet oxygen (1O2), and carbon-centered free radicals (Forootanfara et al. 2013; Torres et al. 2012). This activity of

Fig. 3 Applications of SeNPs Hg

+

Prevents aggregation of COM

Cancer cells

Dissolution of urinary stone (crystals of COM)

Capturing of Hg0 Bioremediation of mercury

Enhancement of chemiluminescence reactions DNBP+ KMNO4 (Dinitrobutylphenol )

Apoptosis induced Anticancer activity

Environment

Acidic conditions

SeNPs enhance reaction

Inactivation of ROS

ROS

CL signal

Antioxidant activity

Nanomedicine

SeNPs

Catalytic activity

H2 O2 Folic acid/transferrin conjugated SeNP

Antimicrobial activity

HRP

Targeted drug delivery

O2

Nanobiosensors Antibacterial activity Antileishmanial activity Antibiofilm activity Antifungal activity Antiplanktonic activity

GC coated with HRP+SeNP

Designing of nanobiosensor

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nanoparticles is size dependent where smaller SeNPs possess higher free radical scavenging potential (Torres et al. 2012). Anticancer activity SeNPs have an anticancer activity against kidney, breast, lung, and osteosarcoma (Ali et al. 2013; Gao and Kong 2011; Ramamurthy et al. 2013; Shakibaie et al. 2010; Yang et al. 2012; Yazdi et al. 2013) and, hence, can be used as chemopreventive and chemotherapeutic agents. Mechanisms for anticancer action are not fully understood; however, several hypotheses have been proposed: (i) enhanced oxidative stress, carcinogen detoxification, and immune surveillance; (ii) induction of cellular and mitochondria-mediated apoptosis; (iii) inhibition of tumor cell invasion and angiogenesis; (iv) cell cycle arrest at S phase; (v) metastasis prevention by inhibition of matrix metalloproteinases expression; and (vi) mobilization of endogenous copper (Ahmad et al. 2015; Chen et al. 2008; Luo et al. 2012; Shakibaie et al. 2010). High level of arsenic (As) in drinking water increases the risk of cancer. SeNPs synthesized from the leaf extract of Terminalia arjuna cast protection against As (III)-induced cell death and DNA damage by minimizing the production of As (III)-induced ROS (Prasad et al. 2013; Prasad and Selvaraj 2014). Oral administration of Lactobacillus brevis along with SeNPs in a metastatic breast cancer mice model stimulates the immune response by increasing the interferon production and delayed-type hypersensitivity response (Yazdi et al. 2012). The mechanism by which SeNPs increase interferon production is unknown. Conjugation of SeNPs with organic molecules and drugs prevents aggregation of the nanoparticles, enhances their anticancer efficacy, and subsides the toxic effects of antibiotics (Ahmad et al. 2015; Li et al. 2011; Ramamurthy et al. 2013; Rezvanfar et al. 2013; Vekariya et al. 2013; Yang et al. 2012). SeNPs linked with Spirulina polysaccharides inhibit the growth of tumor by inducing apoptosis confirmed by an increase in sub G1 cell population, DNA fragmentation, and chromatin condensation. These conjugates also help in targeted delivery of nanoparticles in cancer cells through specific interactions between carbohydrates and lectins present on cell surface (Yang et al. 2012). SeNP-doxorubicin nanoconjugates facilitate the cellular uptake of the antibiotic, thereby augmenting its cytotoxic effects against cancer cells. It has been observed by Yang and colleagues through lactate dehydrogenase activity and cell viability that doxorubicin alone causes 20 % cancer cell death while more than 50 % cell death occurs with combination of SeNPs and doxorubicin (Yang et al. 2012). Cisplatin is an alkylating anticancer drug, causing oxidative stress and DNA cross-linking, which lead to nephrotoxicity and spermatotoxicity. However, SeNPs functionalized with 11-mercapto-1-undecanol reduce nephrotoxicity by inhibiting ROS-mediated apoptosis. Owing to

antioxidant activity, SeNPs can improve the quality of sperms and spermatogenesis when co-administered with cisplatin (Li et al. 2011; Rezvanfar et al. 2013). Anastrozole is an aromatase inhibitor used for breast cancer treatment that shows side effects, such as osteoporosis and bone fracture. However, on conjugation with SeNPs, osteoporosis and bone toxicity are prevented (Vekariya et al. 2013). Nanobiosensors There are only two reports on electrochemical nanobiosensors employing SeNPs for the detection of hydrogen peroxide (H2O2) (Wang et al. 2010; Zhang et al. 2004). Besides, having a high sensitivity, biogenic SeNPs provide optimum conditions to the enzyme to retain its native structure and activity. In a nanobiosensor, the nanoparticles are deposited on a glassy carbon electrode followed by immobilization of HRP onto the SeNPs’ layer. It has been reported that SeNPs’ modified electrode shows good electrocatalytic activity towards H2O2. Biosensors designed using biogenic SeNPs (50–400 nm) have a detection limit of 8 × 10−8 M whereas those with chemically synthesized SeNPs (10 nm) exhibit comparatively a lower detection limit of 9.2 × 10−7 M (Wang et al. 2010; Zhang et al. 2004). Environmental applications Reduction of selenate and selenite to non-toxic elemental Se forms the core to remove the toxic form of Se from the environment (Garbisu et al. 1996; Pickett et al. 2013). Microorganisms present in an anaerobic granular sludge efficiently reduce toxic Se oxyanions to amorphous elemental Se during the treatment of contaminated water. Heating induces the transformation of SeNPs from amorphous to crystalline form, which gets settled and can be easily removed from wastewater (Lenz et al. 2009). E. cloacae SLD1a-1 has been used for the bioremediation of seleniferous compounds from agricultural drainage water (Losi and Frankenberger 1997). The ability of biogenic amorphous SeNPs to sequester reduced mercury (Hg0) is used to remove mercury from contaminated water (Jiang et al. 2012). The botanical specimens in the museum are preserved by mercury salts (e.g., HgCl2), which prevent bacterial contamination by producing mercury vapors (Hg0). However, the Hg0 production is temperature dependent and its concentration rises above safety level in summers. Hence, biogenic amorphous SeNPs can be used to reduce Hg0 level in the long run (Fellowes et al. 2011). Toxicity of SeNPs Biogenic SeNPs are biocompatible and less toxic than selenite and selenate (Benko et al. 2012; Shakibaie et al. 2013; Wang et al. 2007; Zonaro et al. 2015). However, the toxicity of

Appl Microbiol Biotechnol

SeNPs can largely vary among different species (Li et al. 2008). Biogenic SeNPs are reported to be 26-fold less toxic than SeO2 with LD50 of SeO2 and SeNPs 7.3 and 198.1 mg/kg, respectively (Shakibaie et al. 2013). Short-term and sub-acute toxicity experiments on mice revealed the higher toxicity of selenite in comparison to nano Se. Selenite supprsuppresses the growth of mice and affects its liver function by inhibiting catalase and superoxide dismutase activity and increasing malondialdehyde. It also inhibits reduced glutathione and reduces the number of white blood cells, bone marrow cells, and granulocyte macrophages as compared to SeNPs. The order of toxicity for Se compounds is selenate > selenite > SeNPs (Benko et al. 2012). However, in a Se-sufficient Medaka fish, SeNPs are reported to be sixfold more toxic than sodium selenite because of oxidative stress, which may be due to hyperaccumulation of Se in the liver (Li et al. 2008).

Conclusions and future prospects Biogenic SeNPs, synthesized employing microorganisms and plant extracts, have advantages and wide applicability in the field of nanomedicine. Multi-metallic nanoparticles are known to have superior properties than individual metal nanoparticles, and hence, new methods should be developed for the production of biphasic SeNPs, which may have enhanced therapeutic applications. Effect of biological source and physicochemical parameters, such as salt concentration, temperature, pH, aeration, reaction time, etc., should be studied to synthesize SeNPs of size smaller than 100 nm. There are very few reports of such bio-SeNPs and it is still a great challenge for researchers. Size reduction will also increase the activity of nanoparticles and render them more effective. Moreover, combination of different factors may lead to the formation of SeNPs having shapes other than sphere as reported with metal nanoparticles. Reductase enzyme is responsible for the conversion of selenate and selenite to nano Se in bacteria, mostly studied in T. selenatis, E. coli, and E. cloacae. However, the existence of multiple electron transport pathways has not been ruled out. Mechanism of SeNPs synthesis by fungi and plant extracts is poorly understood. Also, how these nanoparticles exhibit an antimicrobial action is still unclear. There are no specificity and comparative studies between chemical and biological SeNPs with respect to the applications. Furthermore, experiments need to be carried out to study the surface functionalization of SeNPs with drugs, which will open new avenues in biomedicine. It is important to explore the potential of biogenic SeNPs as anti-TB and antiviral agents, catalysts, and targeted drug-delivery vehicles.

Acknowledgments SAW and RS acknowledge University Grants Commission (UGC), New Delhi, India, for awarding research fellowship. UUS is thankful to UGC, New Delhi, for awarding UGC-D.S. Kothari Post Doctoral Fellowship. Compliance with ethical standards Conflict of interest The authors declare that they have no competing interests.

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