Interaction of TGA@CdTe Quantum Dots with an Extracellular Matrix of Haematococcus pluvialis Microalgae Detected Using Surface-Enhanced Raman Spectroscopy (SERS)
Restricted accessResearch articleFirst published online September, 2016
Interaction of TGA@CdTe Quantum Dots with an Extracellular Matrix of Haematococcus pluvialis Microalgae Detected Using Surface-Enhanced Raman Spectroscopy (SERS)
The present study reports the localization and interaction of thioglycolic acid (TGA) capped CdTe quantum dots (TGA@CdTe QDs) within the extracellular matrix (ECM) of Haematococcus pluvialis (Chlorophyceae) microalgae (HPM) after an incubation period of 5 min. Changes in the Raman spectrum of HPM induced by the adsorption of the TGA@CdTe QDs are successfully found by using naked gold anisotropic structures as nano-sensors for surface-enhanced Raman scattering (SERS effect). Raman spectroscopy results show that TGA@CdTe QDs interact with the biomolecules present in the ECM. Sample preparation and characterization by complementary techniques such as confocal and electron microscopy are also used to confirm the presence and localization of the nanoparticles in the algae. This research shows new evidence on early accumulation of QDs in plant cells and would further improve our understanding about their environmental impact.
PaulS.PearsonC.MolloyA.CousinsM.GreenM.KolliopoulouS.DimitrakisP.NormandP.TsoukalasD.PettyM.“Langmuir-Blodgett Film Deposition of Metallic Nanoparticles and Their Application to Electronic Memory Structures”. Nano Letters2003; 3(4): 533–536.
2.
SoppimathK.S.AminabhaviT.M.KulkarniA.R.RudzinskiW.E.“Biodegradable Polymeric Nanoparticles as Drug Delivery Devices”. J. Control2001; 70: 1–20.
SkM.P.JaiswalA.PaulA.GhoshS.S.ChattopadhyayA.“Presence of Amorphous Carbon Nanoparticles in Food Caramels”. Scientific Reports2012; 2: 383.
5.
WangT.BaiJ.JiangX.NienhausG.U.“Cellular Uptake of Nanoparticles by Membrane Penetration: A Study Combining Confocal Microscopy with FTIR Spectroelectrochemistry”. ACS Nano2012; 6(2): 1251–1259.
6.
WormsI.A.BoltzmanJ.GarciaM.SlaveykovaV.I.“Cell-Wall-Dependent Effect of Carboxyl-Cdse/Zns Quantum Dots on Lead and Copper Availability to Green Microalgae”. Environ Pollut2012; 167: 27–33.
7.
StewartT. J.SzlachetkoJ.SiggL.BehraR.NachtegaalM.“Tracking the Temporal Dynamics of Intracellular Lead Speciation in a Green Alga”. Environmental Sci. Technol2015; 49(18): 11176–11181.
8.
Yuriel NúñezF.MikhailI. V.“Optical Properties of Bulk and Nanocrystalline Cadmium Telluride”. In: DoneganJ.F.RakovichY.P. (eds). Cadmium Telluride Quantum Dots: Advances and Applications, Singapore: Pan Stanford Publishing, 2013, pp. 1–22.
9.
IyerG.PinaudF.TsayJ.WeissS.“Solubilization of Quantum Dots with a Recombinant Peptide from Escherichia Coli”. Small2007; 3(5): 793–798.
10.
NurunnabiM.ChoK.J.ChoiJ.S.HuhK.M.LeeY.-K.“Targeted Near-IR Qds-Loaded Micelles for Cancer Therapy and Imaging”. Biomaterials2010; 31(20): 5436–5444.
11.
YvonneW.JenniferC.YuriV.“Biocompatibility and Cellular Localisation of CdTe Quantum Dots”. In: DoneganJ.F.RakovichY.P. (eds). Cadmium Telluride Quantum Dots: Advances and Applications, Singapore: Pan Stanford Publishing, 2013, pp. 205–229.
12.
Anthony LeC.AlyonaS.IgorN.“Biological Applications of Cadmium Telluride Semiconductor Quantum Dots”. In: DoneganJ.F.RakovichY.P. (eds). Cadmium Telluride Quantum Dots: Advances and Applications, Singapore: Pan Stanford Publishing, 2013, pp. 173–204.
13.
BoldtK.BrunsO. T.GaponikN.EychmüllerA.“Comparative Examination of the Stability of Semiconductor Quantum Dots in Various Biochemical Buffers”. J. Phys. Chem. B2006; 110(5): 1959–1963.
14.
SchneiderR.WolpertC.GuilloteauH.BalanL.LambertJ.MerlinC.“The Exposure of Bacteria to CdTe-Core Quantum Dots: The Importance of Surface Chemistry on Cytotoxicity”. Nanotechnology2009; 20(22): 225101.
15.
LovrićJ.BazziH.S.CuieY.FortinG.R.WinnikF.M.MaysingerD.“Differences in Subcellular Distribution and Toxicity of Green and Red Emitting CdTe Quantum Dots”. J. Mol. Med2005; 83(5): 377–385.
16.
NikolaiG.“Assemblies of Thiol-Capped CdTe Nanocrystals”. In: DoneganJ.F.RakovichY.P. (eds). Cadmium Telluride Quantum Dots: Advances and Applications, Singapore: Pan Stanford Publishing, 2013, pp. 61–77.
17.
KobayashiM.KurimuraY.TsujiY.“Light-Independent, Astaxanthin Production by the Green Microalga Haematococcus Pluvialis under Salt Stress”. Biotechnology Letters1997; 19(6): 507–509.
18.
BoussibaS.“Carotenogenesis in the Green Alga Haematococcus Pluvialis: Cellular Physiology and Stress Response”. Physiol. Plant2000; 108(2): 111–117.
19.
CollinsA.M.JonesH.D.HanD.HuQ.BeechemT.E.TimlinJ.A.“Carotenoid Distribution in Living Cells of Haematococcus Pluvialis (Chlorophyceae)”. PloS One2011; 6(9): e24302.
20.
KaczorA.TurnauK.BaranskaM.“In Situ Raman Imaging of Astaxanthin in a Single Microalgal Cell”. Analyst2011; 136(6): 1109–1112.
21.
HagenC.SiegmundS.BrauneW.“Ultrastructural and Chemical Changes in the Cell Wall of Haematococcus Pluvialis (Volvocales, Chlorophyta) During Aplanospore Formation”. Eur. J. Phycol2002; 37(2): 217–226.
22.
WayamaM.OtaS.MatsuuraH.NangoN.HirataA.KawanoS.“Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation During Encystment in the Green Alga Haematococcus Pluvialis”. PLOS One2013; 8(1): e53618.
23.
MorelliE.CioniP.PosarelliM.GabellieriE.“Chemical Stability of Cdse Quantum Dots in Seawater and Their Effects on a Marine Microalga”. Aquat. Toxicol2012; 122–123: 153–162.
24.
MorelliE.SalvadoriE.BizzarriR.CioniP.GabellieriE.“Interaction of Cdse/Zns Quantum Dots with the Marine Diatom Phaeodactylum Tricornutum and the Green Alga Dunaliella Tertiolecta: A Biophysical Approach”. Biophys. Chem2013; 182: 4–10.
25.
HanD.WangJ.SommerfeldM.HuQ.“Susceptibility and Protective Mechanisms of Motile and Non Motile Cells of Haematococcus Pluvialis (Chlorophyceae) to Photooxidative Stress”. J. Phycol2012; 48(3): 693–705.
26.
WangY.MiaoA.-J.LuoJ.WeiZ.-B.ZhuJ.-J.YangL.-Y.“Bioaccumulation of CdTe Quantum Dots in a Freshwater Alga Ochromonas Danica: A Kinetics Study”. Environ. Sci. Technol2013; 47(18): 10601–10610.
27.
LinS.BhattacharyaP.RajapakseN.C.BruneD.E.KeP.C.“Effects of Quantum Dots Adsorption on Algal Photosynthesis”. J. Phys. Chem. C2009; 113(25): 10962–10966.
28.
KneippJ.KneippH.KneippK.“SERS—a Single-Molecule and Nanoscale Tool for Bioanalytics”. Chem. Soc. Rev2008; 37(5): 1052–1060.
29.
LeeT.-H.WangH.-Y.“Simultaneous Quantification of Cellular Lipids and Carotenoids inside Chlorella Vulgaris Using Raman Spectrometry”. Energy Procedia2014; 61: 829–833.
30.
KneippK.KneippH.KneippJ.“Surface-Enhanced Raman Scattering in Local Optical Fields of Silver and Gold Nanoaggregates from Single-Molecule Raman Spectroscopy to Ultrasensitive Probing in Live Cells”. Acc. Chem. Res2006; 39(7): 443–450.
31.
GaponikN.TalapinD.V.RogachA.L.HoppeK.ShevchenkoE.V.KornowskiA.EychmüllerA.WellerH.“Thiol-Capping of CdTe Nanocrystals: An Alternative to Organometallic Synthetic Routes”. J. Phys. Chem. B2002; 106(29): 7177–7185.
32.
MartinM.N.BashamJ.I.ChandoP.EahS.-K.“Charged Gold Nanoparticles in Non-Polar Solvents: 10-min Synthesis and 2D Self-Assembly”. Langmuir2010; 26(10): 7410–7417.
33.
HossainM.KitahamaY.HuangG.KanekoT.OzakiY.“SPR and SERS Characteristics of Gold Nanoaggregates with Different Morphologies”. App. Phys. B2008; 93(1): 165–170.
34.
RechtL.ZarkaA.BoussibaS.“Patterns of Carbohydrate and Fatty Acid Changes under Nitrogen Starvation in the Microalgae Haematococcus Pluvialis and Nannochloropsis Sp”. Appl. Microbiol. Biotechnol2012; 94(6): 1495–1503.
35.
GoldsteinA.SorokaY.Frušić-ZlotkinM.PopovI.KohenR.“High Resolution SEM Imaging of Gold Nanoparticles in Cells and Tissues”. J. Microsc. (Oxford, U.K.)2014; 256(3): 237–247.
36.
KrishnaC.M.SockalingumG.KurienJ.RaoL.VenteoL.PluotM.ManfaitM.KarthaV.“Micro-Raman Spectroscopy for Optical Pathology of Oral Squamous Cell Carcinoma”. Appl. Spectrosc2004; 58(9): 1128–1135.
37.
KristoffersenA.S.SvensenØ.SsebiyongaN.ErgaS.R.StamnesJ.J.FretteØ.“Chlorophyll a and NADPH Fluorescence Lifetimes in the Microalgae Haematococcus Pluvialis (Chlorophyceae) under Normal and Astaxanthin-Accumulating Conditions”. Appl. Spectrosc2012; 66(10): 1216–1225.
38.
KneippK.HakaA.S.KneippH.BadizadeganK.YoshizawaN.BooneC.Shafer-PeltierK.E.MotzJ.T.DasariR.R.FeldM.S.“Surface-Enhanced Raman Spectroscopy in Single Living Cells Using Gold Nanoparticles”. Appl. Spectrosc2002; 56(2): 150–154.
39.
SunZ.-Z.DingD.GongQ.ZhouW.XuB.WangZ.-G.“Quantum-Dot Superluminescent Diode: A Proposal for an Ultra-Wide Output Spectrum”. Opt. Quantum Electron1999; 31(12): 1235–1246.
40.
GuoJ.LiuX.GaoH.BieJ.ZhangY.LiuB.SunC.“Highly Sensitive Turn-on Fluorescent Detection of Cartap via a Nonconjugated Gold Nanoparticle–Quantum Dot Pair Mediated by Inner Filter Effect”. RSC Advances2014; 4(52): 27228–27235.
41.
YuW.W.QuL.GuoW.PengX.“Experimental Determination of the Extinction Coefficient of CdTe, CdSe, and CdS Nanocrystals”. Chem. Mater2003; 15(14): 2854–2860.
42.
JaiswalJ.K.MattoussiH.MauroJ.M.SimonS.M.“Long-Term Multiple Color Imaging of Live Cells Using Quantum Dot Bioconjugates”. Nat. Biotechnol2003; 21(1): 47–51.
43.
HaissW.ThanhN.T.AveyardJ.FernigD.G.“Determination of Size and Concentration of Gold Nanoparticles from UV-Vis Spectra”. Anal. Chem2007; 79(11): 4215–4221.
44.
KhlebtsovN.G.“Determination of Size and Concentration of Gold Nanoparticles from Extinction Spectra”. Anal. Chem2008; 80(17): 6620–6625.
45.
FranckF.JuneauP.PopovicR.“Resolution of the Photosystem I and Photosystem II Contributions to Chlorophyll Fluorescence of Intact Leaves at Room Temperature”. Biochim. Biophys. Acta, Bioenerg2002; 1556(2–3): 239–246.
46.
RégnierP.BastiasJ.Rodriguez-RuizV.Caballero-CaseroN.CaballoC.SiciliaD.FuentesA.MaireM.CrepinM.LetourneurD.“Astaxanthin from Haematococcus Pluvialis Prevents Oxidative Stress on Human Endothelial Cells without Toxicity”. Mar. Drugs2015; 13(5): 2857–2874.
47.
WuZ.ZhuY.HuangW.ZhangC.LiT.ZhangY.LiA.“Evaluation of Flocculation Induced by Ph Increase for Harvesting Microalgae and Reuse of Flocculated Medium”. Bioresour. Technol2012; 110: 496–502.
48.
TatyanaA.Min SeokK.Jong WonH.TaizoM.ChikakoN.Gwang HoonK.“Cold-Tolerant Strain of Haematococcus Pluvialis (Haematococcaceae, Chlorophyta) from Blomstrandhalvøya (Svalbard)”. Algae2013; 28(2): 185–192.
49.
HeraudP.BeardallJ.McNaughtonD.WoodB.R.“In Vivo Prediction of the Nutrient Status of Individual Microalgal Cells Using Raman Microspectroscopy”. FEMS Microbiol. Lett2007; 275(1): 24–30.
50.
WoodB.R.HeraudP.StojkovicS.MorrisonD.BeardallJ.McNaughtonD.“A Portable Raman Acoustic Levitation Spectroscopic System for the Identification and Environmental Monitoring of Algal Cells”. Anal. Chem2005; 77(15): 4955–4961.
51.
CaiZ.-L.ZengH.ChenM.LarkumA.W.“Raman Spectroscopy of Chlorophyll D from Acaryochloris Marina”. Biochim. Biophys. Acta, Bioenerg2002; 1556(2–3): 89–91.
De GelderJ.De GussemK.VandenabeeleP.MoensL.“Reference Database of Raman Spectra of Biological Molecules”. J. Raman Spectrosc2007; 38(9): 1133–1147.
56.
KaczorA.BaranskaM.“Structural Changes of Carotenoid Astaxanthin in a Single Algal Cell Monitored in Situ by Raman Spectroscopy”. Anal. Chem2011; 83(20): 7763–7770.
57.
PilátZ.BernatováS.JežekJ.ŠeryM.SamekO.ZemánekP.NedbalL.TrtílekM.“Raman Microspectroscopy of Algal Lipid Bodies: β-Carotene Quantification”. J. Appl. Phycol2012; 24(3): 541–546.
58.
UragamiC.YamashitaE.GallA.RobertB.HashimotoH.“Application of Resonance Raman Microscopy to in Vivo Carotenoid”. Acta Biochim. Pol2012; 59(1): 53–56.
59.
MerlinJ.C.“Resonance Raman Spectroscopy of Carotenoids and Carotenoid-Containing Systems”. Pure Appl. Chem1985; 57(5): 785–792.
60.
DementjevA.KostkevičieneJ.“Applying the Method of Coherent Anti-Stokes Raman Microscopy for Imaging of Carotenoids in Microalgae and Cyanobacteria”. J. Raman Spectrosc2013; 44(7): 973–979.
61.
KimJ.S.KukE.YuK.N.KimJ.-H.ParkS.J.LeeH.J.KimS.H.ParkY.K.ParkY.H.HwangC.-Y.“Antimicrobial Effects of Silver Nanoparticles”. Nanotechnol. Biol. Med2007; 3(1): 95–101.
62.
VladimirL.NikolaiG.AlexanderE.“Aqueous Synthesis of Colloidal CdTe Nanocrystals”. In: DoneganJ.F.RakovichY.P. (eds). Cadmium Telluride Quantum Dots: Advances and Applications, Singapore: Pan Stanford Publishing, 2013, pp. 23–59.
63.
CuiX.LiuM.LiB.“Homogeneous Fluorescence-Based Immunoassay Via Inner Filter Effect of Gold Nanoparticles on Fluorescence of CdTe Quantum Dots”. Analyst2012; 137(14): 3293–3299.
64.
AlbaneseA.ChanW.C.“Effect of Gold Nanoparticle Aggregation on Cell Uptake and Toxicity”. ACS Nano2011; 5(7): 5478–5489.
65.
MakJ.S.FarahA.A.ChenF.HelmyA.S.“Photonic Crystal Fiber for Efficient Raman Scattering of CdTe Quantum Dots in Aqueous Solution”. ACS Nano2011; 5(5): 3823–3830.
66.
ZhaoJ.ZhangZ.YuZ.HeZ.YangS.JiangH.“Nucleation and Characterization of Hydroxyapatite on Thioglycolic Acid-Capped Reduced Graphene Oxide/Silver Nanoparticles in Simplified Simulated Body Fluid”. Appl. Surf. Sci2014; 289: 89–96.
67.
Josè-EstanyolM.PuigdomènechP.“Plant Cell Wall Glycoproteins and Their Genes”. Plant Physiol. Biochem2000; 38(1–2): 97–108.
68.
GalatA.“Study of the Raman Scattering and Infrared Absorption Spectra of Branched Polysaccharides”. Acta Biochim. Pol1980; 27(2): 135–142.
69.
CoulonJ.ThouveninI.AldeekF.BalanL.SchneiderR.“Glycosylated Quantum Dots for the Selective Labelling of Kluyveromyces Bulgaricus and Saccharomyces Cerevisiae Yeast Strains”. J. Fluoresc2010; 20(2): 591–597.
