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Nanotubes of Biomimetic Supramolecules Constructed by Synthetic Metal Chlorophyll Derivatives Sunao Shoji, Tetsuya Ogawa, Takeshi Hashishin, Shin Ogasawara, Hiroaki Watanabe, Hisanao Usami, and Hitoshi Tamiaki Nano Lett., Just Accepted Manuscript • DOI: 10.1021/acs.nanolett.6b00781 • Publication Date (Web): 12 May 2016 Downloaded from http://pubs.acs.org on May 16, 2016

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Nanotubes of Biomimetic Supramolecules Constructed by Synthetic Metal Chlorophyll Derivatives Sunao Shoji,*,† Tetsuya Ogawa,‡ Takeshi Hashishin,§ Shin Ogasawara,† Hiroaki Watanabe,† Hisanao Usami|| and Hitoshi Tamiaki*,†

†

Graduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577,

Japan ‡

Institute for Chemical Research, Kyoto University, Uji, Kyoto 611-0011, Japan

§

Faculty of Engineering, Kumamoto University, Kumamoto, Kumamoto 860-8555,

Japan ||

Faculty of Textile Science and Technology, Shinshu University, Ueda, Nagano

386-8567, Japan

Received:

February, 2016

Revised:

April, 2016

1 ACS Paragon Plus Environment

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ABSTRACT: Various supramolecular nanotubes have recently been built up by lipids, peptides and other organic molecules.

Major light-harvesting (LH) antenna systems

in a filamentous anoxygenic phototroph, Chloroflexus (Cfl.) aurantiacus, are called chlorosomes and contain photofunctional single-wall supramolecular nanotubes with approximately 5 nm in their diameter.

Chlorosomal supramolecular nanotubes of Cfl.

aurantiacus are constructed by a large amount of bacteriochlorophyll(BChl)-c molecules.

Such a pigment self-assembles in a chlorosome without any assistance

from the peptides, which is in sharp contrast to the other natural photosynthetic LH antennas.

To mimic chlorosomal supramolecular nanotubes, synthetic models were

prepared by the modification of naturally occurring chlorophyll(Chl)-a molecule. Metal complexes (magnesium, zinc and cadmium) of the chlorophyll derivative were synthesized as models of natural chlorosomal BChls.

These metal Chl derivatives

self-assembled in hydrophobic environments and their supramolecules were analyzed by spectroscopic and microscopic techniques.

Cryo-transmission electron

microscopic images showed that the zinc and cadmium Chl derivatives could form single-wall supramolecular nanotubes and their outer and inner diameters were approximately 5 and 3 nm, respectively.

Atomic force microscopic images suggested

that the magnesium Chl derivative formed similar nanotubes to those of the corresponding zinc and cadmium complexes.

Three chlorosomal single-wall

supramolecular nanotubes of the metal Chl derivatives were prepared in the solid state and would be useful as photofunctional materials.

KEYWORDS: AFM, Chlorophyll, Chlorosome, Cryo-TEM, Self-assembly, Single-wall nanotube, Supramolecule


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Tube-shaped nanomaterials have attracted much attention for the development of electronic devices, material storages, sensors, probes and other applications1 and a variety of organic2–6 and inorganic nanotubes7–9 have been prepared recently. Self-assembly based on molecular interactions (hydrogen bonding, coordination bonding, hydrophobic interaction, π-π stacking, and so on) is useful in the construction of the supramolecular nanotubes.

Various supramolecular nanotubes have been

prepared by lipids, peptides and other organic molecules, and are expected to be functional soft materials and useful in biotechnologies.3 Major light-harvesting (LH) antenna systems in a filamentous anoxygenic phototroph, Chloroflexus (Cfl.) aurantiacus, contain the photofunctional single-wall tubular supramolecules.

Such LH antenna apparatuses are called chlorosomes and

are attractive from the viewpoints of their unique supramolecular structures and optical functions.10,11

Chlorosomes are also seen in main LH antennas of green sulfur

photosynthetic bacteria.

Chlorosomes are large ellipsoidal antenna apparatuses

compared to the other natural LH antennas and chlorosomes in Cfl. aurantiacus were approximately 100, 30 and 15 nm in size along the long, middle and short axes, respectively.12

Such large chlorosomal LH antennas allow green photosynthetic

bacteria to live in extremely low light environments.

For instance, a sort of green

sulfur bacteria can live at up to a 150 m depth under the seawater surface.13 Natural photosynthetic organisms utilize the sunlight for their survival and growth. In the primary process of natural photosynthesis, LH antennas act as absorbing sunlight, migrating the excited energy and transferring the harvested energy to a charge-separating system.

Natural photosynthetic LH antennas contain several

pigments such as (bacterio)chlorophylls [(B)Chls], bilins, carotenoids and quinones. Chl and BChl pigments are the most important photosynthetically active molecules in


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nature and play key roles in the above photophysical functions.14

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Chlorosomes are

constructed by a large amount of BChl-c, d and e molecules (Scheme 1, left), approximately 1–2 × 105 molecules per chlorosome, and these pigments are surrounded by a lipid monolayer.12

These BChl-c, d and e molecules self-assemble without any

assistance from the peptides in a hydrophobic environment,15 which is in sharp contrast to the other natural photosynthetic antennas whose Chls and BChls are located in a specific array by binding with peptides.16

Chlorosomes of Cfl. aurantiacus are

composed of BChl-c pigments, and their freeze fracture transmission electron microscopic (TEM) images showed that in vivo self-assemblies of BChl-c in a chlorosome were rod-shaped supramolecular nanostructures with 5 nm in the diameter.17,18

We have already reported that in vitro 5-nm rod supramolecules were

reconstructed by naturally occurring BChl-c from Cfl. aurantiacus in a hexane-based solution.19

Molecular modelling showed the tube-shaped supramolecule of

self-assembled BChl-c with 5 nm in the diameter20 as well as the self-assembly of a BChl-d derivative whose radius was 2.7 nm in the supramolecular nanotubes.21

It

should be noted that supramolecular structures of BChl self-assemblies in chlorosomes are still in discussion and would be dependent on their molecular structures and additional species including carotenoids, quinones and lipids.

Ten-nm rod

self-assemblies were observed in chlorosomes of green sulfur bacteria, Chlorobaculum (Cba.) tepidum and purvum, by freeze fracture TEM images,18 and multicylindrical and lamellar self-assemblies with their layer spaces of approximately 2 nm were visible in cryo-TEM images of chlorosomes of Cba. tepidum22 and their mutants.23,24 To harness the sunlight energy for our lives, it is valuable to mimic such natural chlorosomal supramolecular nanotubes.

Chlorosomal BChls are magnesium

complexes of 31-hydroxy-131-oxo-chlorins and chemically programmed pigments for


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chlorosomal J-aggregation.

Central metal as well as peripheral 31-hydroxy and

13-keto groups are requisite for chlorosomal intermolecular interactions: coordination bonding (Mg···OH) and hydrogen bonding (OH···O=C) as well as chlorin π-π stacking.25

Synthetic model compounds of such chlorosomal BChl pigments have

been prepared from naturally occurring Chl-a by our group.26

Several metals were

inserted in the center of the chlorin macrocycle and spectroscopic experiments showed central magnesium, zinc and cadmium complexes were useful to prepare chlorosomal self-assemblies.27 Würthner and his colleagues first reported that artificial chlorosomal rod-shaped supramolecular nanostructures with 5 nm in a diameter were prepared by zinc Chl derivatives possessing highly lipophilic substituents.28,29

Such rod-shaped

supramolecules were prepared by evaporating a solution of the zinc Chls on a hydrophobic substrate, highly oriented pyrolytic graphite (HOPG).

Cryo-TEM

analysis showed that water-soluble self-assemblies of zinc Chl possessing a hydrophilic substituent were visible as tube-shaped nanostructures with approximately 6 and 2 nm in outer and inner diameters, respectively.29,30

We reported the rod-shaped

supramolecules with 5 nm in a diameter prepared in a hydrophobic hexane-based solution by structurally simple zinc Chl models possessing an oligomethylene chain at the 17-propionate residue.31

A suspension of the solid rod self-assemblies of zinc Chl

possessing dodecyl ester Zn-1 (Scheme 1, right) were cast on several substrates: HOPG, mica and quartz substrates as well as a carbon coated copper grid.

The solid rod

supramolecular nanostructures were visible in AFM and TEM images.

Here we

report that chlorosomal nanotubes were constructed by self-assemblies of magnesium, zinc and cadmium Chl derivatives.

Single-wall nanotubes with approximately 5-nm

outer and 3-nm inner diameters were visible in cryo-TEM images of self-assemblies of


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zinc and cadmium complexes.

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AFM images showed that rod-shaped nanostructures

with 5 nm in the height were observed by self-assemblies of the magnesium complex which were comparable nanostructures to those of Zn- and Cd-Chls, and suggested that similar single-wall nanotubes were prepared in the solid state by the three metal Chl derivatives. Preparation of chlorosomal supramolecules. Metal-free chlorin H2-1 (M = H2 in Scheme 1, right) was synthesized by the modifications of naturally occurring Chl-a from cyanobacterial spirulina powder according to the reported procedure.31

Metal

complexes of the Chl derivative M-1 (M = Mg, Zn and Cd; Scheme 1, right) were synthesized by the metallation27 of H2-1.

All the metal Chls were characterized by

their nuclear magnetic resonance (NMR), high resolution mass (HRMS) as well as ultraviolet, visible and near-infrared (UV-Vis-NIR) absorption spectra (see Supporting Information). UV-Vis-NIR absorption spectra of monomeric M-1 (M = Mg, Zn and Cd) in tetrahydrofuran (THF) showed Qy bands at 653, 647 and 650 nm and Soret bands at 431, 424 and 427 nm, respectively (thin lines in Figure 1, upper).

Self-assemblies of

Mg-1, Zn-1 and Cd-1 in 1%(v/v) THF and hexane (10 µM) showed Qy/Soret maxima at 752/453, 740/450 and 732/455 nm (thick lines in Figure 1, upper).

The Qy

absorption band of Cd-1 self-assemblies showed a shoulder band at around 700 nm. It seemed that the cadmium complex formed two oligomeric species in a solution. Exciton-coupled CD signals of self-assemblies of metal Chl derivatives were also observed in the Qy region and the shapes of these signals were similar to each other (Figure 1, lower).

These spectroscopic evidences indicate the metal complexes

formed J-aggregates and were closely similar to the natural chlorosomal self-assemblies.


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Self-assembled solids of synthetic metal Chl derivatives were prepared according to the reported procedures.19,31

The solutions of Mg-1 and Zn-1 in THF (10 mM)

were added to 99-fold hexane to give their precipitates.

Self-assemblies of Cd-1 were

prepared by the following due to its lower solubility in THF than Mg-1 and Zn-1. The solution of Cd-1 in THF (2 mM) was added to 95-fold hexane to give precipitates. Each solution was allowed to stand in the dark at room temperature for 7 days.

The

self-assembled solids were dispersed by ultrasound irradiation and the resulting suspensions were adsorbed on quartz substrates.

UV-Vis-NIR absorption spectra of

the self-assemblies of Mg-1, Zn-1 and Cd-1 on quartz showed at 747-, 733- and 730-nm Qy absorption peaks and 451-, 445- and 453-nm Soret absorption maxima (Figure S1). UV-Vis-NIR absorption spectra of the self-assemblies on a quartz were closely similar to those of the solution state.

Therefore, solid supramolecules of the metal Chl

derivatives were prepared in a chlorosomal well-ordered manner and were stable in air and at room temperature during the measurements. Observation of chlorosomal supramolecular nanotubes. The suspensions of chlorosomal supramolecular solids were drop-cast on a carbon coated copper grid and analyzed by cryo-TEM.

Cryo-TEM was applied for reduction of electron beam

damage of the samples and their microstructural observation at high resolution. Cryo-TEM images of self-assemblies of Zn-1 and Cd-1 are shown in Figure 2, where supramolecular nanotubes were apparently visible.

The outer and inner diameters of

the supramolecular nanotubes of Zn-1 were 4.8~6.2 and 2.3~3.5 nm (Figure 2, upper), and their outer diameter was similar to the previously reported rod-shaped nanostructures

observed

by

tapping-mode

AFM

and

conventional

TEM.31

Additionally, both the inner and outer diameters were also closely similar to those of the reported water-soluble Chl supramolecular nanotubes.29,30


Cryo-TEM analysis

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showed more detailed nanostructures of self-assembled Zn-1 which were previously observed as rods by AFM and conventional TEM.31

Cd-1 also formed nanotubes

with 5.0 and 2.5 nm in outer and inner diameters, respectively (Figure 2, lower), so that a supramolecular arrangement of these Cd-1 nanotubes would be similar to those of Zn-1.

Furthermore, other nanotubes with 3.7~4.0-nm outer and 0.8~1.5-nm inner

diameters were also visible in a cryo-TEM image of self-assemblies of Cd-1.

Such a

smaller size of nanotubes was not observed in a cryo-TEM image of self-assemblies of Zn-1.

As mentioned above, self-assemblies of Cd-1 in a diluted solution, 1%(v/v)

THF–hexane, showed another oligomeric species possessing a Qy absorption band at around 700 nm.

Such oligomeric Cd-1 might result in the formation of nanotubes

with smaller inner and outer diameters.

Self-assemblies of Cd-1 were also examined

by conventional TEM without stain.

The TEM image showed the presence of

nanotubes with 5 and 3 nm in widths, while the inner space was not visible in the low-resolution TEM image (Figure S2).

Energy dispersive X-ray spectrum indicated

the presence of the cadmium element, which suggested the nanotubes were composed of self-assemblies of Cd-1.

Neither nanotubes nor rods of self-assembled Mg-1 were

visible in stain-free cryo-TEM and conventional TEM images, which would be due to its light magnesium element. The suspension of the self-assemblies of Chl metal complexes were drop-cast on an HOPG substrate and analyzed by tapping-mode AFM.

Figure 3 shows AFM

images and their cross-section analyses of chlorosomal supramolecules of Mg-1 and Cd-1.

The height and length of the rods of self-assembled Cd-1 were 5.2 and 255 nm,

and those of self-assembled Mg-1 were 5.1 and 200 nm, respectively (Figures 3a–f). These rod supramolecular nanostructures with a 5-nm height in AFM images of Cd-1 and Mg-1 self-assemblies were identical to those previously reported for Zn-1.31


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Moreover, these rods were closely similar to the nanotubes of self-assemblies of Zn-1 and Cd-1 observed by cryo-TEM.

Five-nm height of the rods was similar to the outer

diameter of nanotubes observed by cryo-TEM.

Therefore, rod-shaped nanostructures

in AFM images are similar to the nanotubes observed by cryo-TEM.

Tube-shaped

nanostructures of self-assemblies of Mg-1 were not observed by cryo-TEM, but a rod with a 5-nm height was observed by AFM, which suggests supramolecules of Mg-1 were also similar nanotubes to those of Zn-1 and Cd-1.

Supramolecular structures of

these nanotubes observed in cryo-TEM and AFM images would be similar to those of the molecular modeling.20,21

Tubes with 2~3 nm in a height were also visible in an

AFM image of Cd-1 self-assemblies (Figures 3g and h), which were also visible in a cryo-TEM image.

The other long tube-like nanostructures with ~5-nm and 7~10-nm

heights were observed in an AFM image of Mg-1 self-assemblies (Figures 3i and j), which were closely similar to supramolecular nanostructures of in vitro self-assemblies of naturally occurring BChl-c from Cfl. aurantiacus.19

It seemed that the 31- and

20-methyl groups of BChl-c did not largely affect the in vitro chlorosomal supramolecular nanostructures. A schematic drawing of a chlorosomal supramolecular nanotube with 5-nm outer and 3-nm inner diameters observed is shown in Figure 4.

The present biomimetic

nanotubes are promising for photofunctional materials.

The suspension of the

self-assemblies of Zn-1 was drop-cast on an ITO electrode, and an AFM image showed the presence of the nanotube with a 5-nm height on the ITO electrode (Figure S3).

It

is noted that photoexcited chlorosomal supramolecular nanotubes on an ITO or TiO2 electrode in an aqueous buffer solution generated a cathodic or anodic photocurrent, respectively (see Figures S4–6 and experimental details in Supporting Information), which was similar to the reported photoelectron conversions of synthetic Chl derivative


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and natural BChl-c self-assemblies as well as isolated natural chlorosomes.32–37 Conclusion. Magnesium, zinc and cadmium complexes of a Chl derivative were synthesized from naturally occurring Chl-a as models of natural chlorosomal BChls. Supramolecules of the three metal Chl derivatives were analyzed by spectroscopic and microscopic techniques.

UV-Vis-NIR absorption and CD spectra showed these metal

Chls self-assembled in a hydrophobic hexane-based solution.

Optical properties of

self-assemblies of their metal complexes on quartz were closely similar to each other. Supramolecular nanotubes of zinc and cadmium complexes were visible in cryo-TEM images.

Their outer and inner diameters were approximately 5 and 3 nm, respectively.

AFM images suggested the magnesium complex also self-assembled to form similar nanotubes as zinc and cadmium Chls.

Another nanotubes were visible in cryo-TEM

and AFM images of self-assemblies of Cd-1 and their outer and inner diameters were approximately 3 and 1 nm, respectively.

The other supramolecular tube-like

nanostructures were observed in an AFM image of self-assemblies of Mg-1. Nanotubes with a similar diameter were successfully prepared in the solid states of the three metal Chl self-assemblies, and would be similar supramolecular nanostructures to BChl-c self-assemblies in a chlorosome of Cfl. aurantiacus.

The present

supramolecular nanotubes of metal Chls are reminiscent of covalently built carbon nanotubes which have been widely investigated for commercial application.38 Natural chlorosomal supramolecules are highly photofunctional apparatuses, thus these present biomimetic nanotubes would be useful for artificial photosynthetic systems and also as novel photonics materials for nanotechnologies.

ASSOCIATED CONTENT Supporting Information


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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.nano-lett.xxxxxxx, including experimental details, synthetic procedures, spectral data of M-1 and TEM analysis of Cd-1 as well as photocurrent measurements of M-1.

AUTHOR INFORMATION Corresponding Authors *E-mail: [email protected] *E-mail: [email protected] Notes The authors declare no competing financial interest.

ACKNOWLEDGEMENTS This work was partially supported by Grants-in-Aid for Scientific Research on Innovative Areas “Artificial photosynthesis (AnApple)” (No. 24107002, to H. Tamiaki) from the Japan Society for the Promotion of Science (JSPS) as well as for JSPS Fellows (26-8467, to S. Shoji). A part of this work was supported by Kyoto University Nano Technology Hub in “Nanotechnology Platform Project” sponsored by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan. We thank Prof. Hiroki Kurata, Kyoto University, for observation of cryo-TEM images and Prof. Hideyuki Takakura, Ritsumeikan University, for measurements of photocurrent action spectra.


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Captions for drawings

Scheme 1. Molecular structures of naturally occurring BChls-c, d and e (R8 = Me, Et, Pr, i-Bu; R12 = Me, Et; R17 = cetyl, geranylgeranyl, oleyl, phytyl, stearyl for filamentous anoxygenic phototrophs; R17 = farnesyl for green sulfur bacteria) and metal Chl derivatives M-1 (M = Mg, Zn and Cd) as their synthetic models.

Figure 1. UV-Vis-NIR absorption (upper) and CD spectra (lower) of metal Chl derivatives Mg-1 (solid lines), Zn-1 (dotted lines) and Cd-1 (dashed lines) in THF (thin lines) and self-assemblies in 1%(v/v) THF–hexane (thick lines).

Figure 2. Cryo-TEM images of chlorosomal self-assemblies of (a) Zn-1 and (b) Cd-1 on a carbon coated copper grid.

Figure 3. AFM images and cross-section analysis of chlorosomal self-assemblies of Cd-1 (a–c, g and h) and Mg-1 (d–f, i and j) on HOPG.

Figure 4. Schematic drawing of chlorosomal supramolecular nanotubes of metal Chl derivatives with 5-nm outer and 3-nm inner diameters.


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Scheme 1 S. Shoji, et al.


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Figure 1 S. Shoji, et al.


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Graphical Abstract S. Shoji, et al.


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Scheme 1. Molecular structures of naturally occurring BChls-c, d and e (R8 = Me, Et, Pr, i-Bu; R12 = Me, Et; R17 = cetyl, geranylgeranyl, oleyl, phytyl, stearyl for filamentous anoxygenic phototrophs; R17 = farnesyl for green sulfur bacteria) and metal Chl derivatives M-1 (M = Mg, Zn and Cd) as their synthetic models. 64x49mm (300 x 300 DPI)

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Figure 1. UV-Vis-NIR absorption (upper) and CD spectra (lower) of metal Chl derivatives Mg-1 (solid lines), Zn-1 (dotted lines) and Cd-1 (dashed lines) in THF (thin lines) and self-assemblies in 1%(v/v) THF–hexane (thick lines). 83x115mm (300 x 300 DPI)


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Figure 2. Cryo-TEM images of chlorosomal self-assemblies of (a) Zn-1 and (b) Cd-1 on a carbon coated copper grid. 163x319mm (300 x 300 DPI)


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Figure 3. AFM images and cross-section analysis of chlorosomal self-assemblies of Cd-1 (a–c, g and h) and Mg-1 (d–f, i and j) on HOPG. 158x299mm (300 x 300 DPI)


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Figure 4. Schematic drawing of chlorosomal supramolecular nanotubes of metal Chl derivatives with 5-nm outer and 3-nm inner diameters. 83x83mm (300 x 300 DPI)


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Abstract Graphic 81x44mm (300 x 300 DPI)


Nanotubes of Biomimetic Supramolecules ... - ACS Publications

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