Self-organizing colours of butterflies

Updating Magic Universe

Self-organizing colours of butterflies

The papilionid Emerald-patched Cattleheart, Parides sesostris. Source: Richard Prum

A multi-disciplinary study at Yale, by evolutionary biologists, physicists and various kinds of engineers, aided by X-ray scattering specialists at the Argonne National Laboratory, has clarified the way in which butterfly wings generate shimmering colours. The wings employ a physical trick of the light that’s more influential than any chemical pigments. The team, led by biologist Richard Prum, has published the findings in this week’s on-line issue of the Proceedings of the National Academy of Sciences.

A gyroid, as visualized by Alan Schoen. Image from NASA

Complex curved assemblies of molecules called gyroids do the trick, by scattering light in distinctive ways that depend on the dimensions of the gyroids, the slant of incoming light, and the angle of view. Digging a little, I find that a mathematician, Alan Schoen, discovered gyroids as possible shapes, long before their biological role was known. In 1970, while at the Electronics Research Center in Cambridge, Massachusetts, Schoen wrote a paper for NASA that began: “A preliminary account of a study of the partitioning of three-dimensional Euclidean space into two interpenetrating labyrinths by intersection-free infinite periodic minimal surfaces …” Key words there are “labyrinths” and “periodic”.

But how does a butterfly, however mathematically astute, set about building its gyroids?  According to Prum and his chums, the outer membrane of a cell in the butterfly’s wing folds into the cell’s interior from above and below to make a double gyroid. Then starchy chitin forms on the outer gyroid to solidify it before the cell dies – leaving the colour-generating crystal form on the surface of the wing.

Here’s the most relevant story in Magic Universe. It’s called “Molecular partners: letting natural processes do the chemist’s work”.

Strasbourg or Strassburg lies in the rift valley between the Vosges and the Schwarzwald, down which the Rhin or Rhein pours. The city is closer to Munich than to Paris, and repeated exchanges of territory between the French and the Germans aggravated an identity problem of the people of Alsace. It was not resolved until, after restoration to France in 1945, Strasbourg became a favoured locale for Europe-wide institutions. But history left the Alsatians better able than most to resist the brain drain to Paris, and to pursue their own ideas, whether with dogs, pottery or science.

As a 28-year-old postdoc in Strasbourg, Jean-Marie Lehn embarked in 1967 on a new kind of chemistry that was destined to become a core theme of 21st-Century research worldwide. It would straddle biology, physics and engineering. As it concerned not individual molecules, made by bonding atoms together, but the looser associations and interactions between two or more molecules, he called the innovation supramolecular chemistry.

Lehn had spent a year at Harvard contributing in a junior role to a tour de force of molecular chemistry, when Robert Woodward and a large team of researchers synthesized vitamin B12. It was the most complex molecule ever produced from scratch. Whilst technically instructive, in the latest arts of laboratory synthesis, the experience was thought provoking. Need chemistry be so difficult?

A philosophical interest in how the brain worked at the most basic chemical level, by controlling the passage of charged atoms (ions) of sodium and potassium through the walls of nerve cells, prompted Lehn to investigate materials capable of acting as carriers to transport these ions through biological membranes. Natural ring-shaped antibiotics are one category of such substances. Charles Pedersen in the DuPont lab in Delaware discovered another category, the crown ethers. These are rings of carbon and oxygen atoms in the shape of a crown, and they can firmly lasso ions of lithium, sodium, potassium, rubidium or caesium.

Lehn developed a third type, hollow cage-like molecules capable of strongly catching ions in a 3-D internal cavity, thus forming species that he called cryptates. These were much more selective in the metal guests, the choice of which depended on the sizes of their ions as compared with the sizes of the cavities. Lehn went on to devise molecules adapted to gathering whole molecules into cavities and clefts in their 3-D structures.

At that time, molecular biologists were revealing that enzymes, the proteins that catalyse biochemical reactions in living cells, operate that way. As brilliantly predicted by Emil Fischer of Berlin in 1899, the molecule being processed fits precisely into an enzyme molecule like a lock into a key. This association, based on the correct fitting between the partners, was what Lehn had in mind when he set out to make supramolecular assemblies of synthetic materials showing such molecular recognition.

When two atoms join together with a permanent bond, like that between the hydrogen and oxygen atoms in water, the product is a molecule. In a supermolecule the connection remains looser, like that between the water molecules in ice. And just as ice can melt, so a supermolecule can rather easily fall to pieces again.

New lines of research developed, as Lehn set himself the aim of engineering artificial molecules into ‘molecular devices’. Using their ability to recognize, transport and modify target molecules, they should be able to perform signalling and information-processing operations on an incredibly small scale. And Lehn expected that the manufacture of chemical machines would rely heavily on the ability of molecules to assemble themselves into well-defined superstructures, a process called supramolecular self-organization.

Molecular moulds and casts

By 1996 Lehn was on the way to bringing natural selection into play among self-organizing molecules, to select those fittest for their purpose. A young chemist working with him at Strasbourg, Bernold Hasenknopf, found that artificial ring shaped molecules were able to adapt their size reversibly to fit species present in the medium. Thereafter, another collaborator, Ivan Huc, presented a mixture of small synthetic molecules, called aldehydes and amines, to a well-known natural enzyme, carbonic anhydrase. It could just as well have been a man-made molecule with a cavity, but it’s easier to buy enzymes off the shelf.

The small molecules spontaneously formed the supramolecular assembly that best fitted into the cleft of the enzyme. To understand what was new here, consider that a biologist might be interested in how carbonic anhydrase evolved its cleft to suit the natural molecule that it processes. From the opposite starting point, a chemist working traditionally, perhaps to find a drug that might inhibit an enzyme, would synthesize many different molecules and test them one by one to see whether, by good luck, any fitted the cleft well.

Huc and Lehn, by contrast, relied on random connections among the small molecules to make assemblies that would test themselves in the enzyme. The continuous generation of all possible partnerships among the molecular components made available every structural feature and capacity for supramolecular interaction latent in the mixture. Those assemblies that didn’t fit the enzyme clefts very well retreated from the scene.

Gradually, the enzyme molecules filled up with supramolecular assemblies that fitted them snugly. This was the chemical equivalent of casting from a concave mould. Conversely, the process studied earlier by Hasenknopf amounted to molding a supramolecular cavity around a convex molecule of choice.

‘Both processes also amount to the generation of the fittest,’ Huc and Lehn commented, ‘and [they] present adaptation and evolution by spontaneous recombination under changes in the partners or in the environmental conditions. They thus embody a sort of supramolecular Darwinism!’

At the end of the century Lehn was running the Institut de Science et d’Ingénierie Supramoléculaires in Strasbourg, and a parallel operation at the Collège de France in Paris. Other laboratory projects for supramolecular research sprang up all around the world. A flurry of scientific meetings, books and journal articles confirmed that a new branch of science was in the making.

Spinning molecules and shell patterns

A hint of things to come appeared in 1998, in the form of a molecular rotor, devised at IBM’s Zurich Research Laboratory with participation from Denmark’s Risø National Laboratory. James Gimzewski and his colleagues laid a layer of screw-shaped molecules called hexabutyl decacyclene on a copper surface. They mostly arranged themselves in a static hexagonal pattern, but in some places there were voids about 2 millionths of a millimetre wide, within which one molecule had separated from its neighbours. It rotated at high speed, with the surrounding molecules acting as a frictionless bearing.

‘Our rotor experiment opens the way to making incredibly small supramolecular motors,’ Gimzewski said. ‘And it’s interesting that we’re pushing at limits set by the laws of heat, which rule out perpetual motion machines. In the initial experiment the rotors turned in either direction. To have a molecule turning only one way, to give useful work, we have to put energy into the system. But we can still expect efficiencies close to the theoretical maximum.’

Although the ability of natural enzymes to form temporary associations with other materials was an important inspiration concerning molecular partnerships, the chemists’ ideas about supramolecular interactions feed back into biology. For example the prolific diatoms, often called the jewels of the sea, are single-celled algae with beautiful symmetrical patterns in their shells. These are distinctive enough to allow marine biologists and fossil hunters to tell apart many thousands of diatom species. Manfred Sumper of Regensburg worked out how the diatoms build their shells by supramolecular chemistry.

Here the partnership involves long-chain molecules, polyamines, and the silica that builds the shells. The polyamines form droplets or micelles that arrange themselves in a hexagonal pattern. These gather the silica around them, so that it forms a honeycomb shell. Polyamines are consumed in the process, and the droplets break up, continuing the pattern making down to ever-smaller scales. ‘The eventual patterns in the diatom shells seem to depend primarily on the length of the polyamine chain used by each species,’ Sumper concluded.

A staggering agenda

In Strasbourg, Jean-Marie Lehn kept his eye firmly on the long-term future. Everything that had happened in surpramolecular research so far was, in his opinion, just a rehearsal for far greater possibilities to come. He summed them up in a string of adjectives, in writing of ‘complex, informed, self-organized evolutive matter’.

By ‘informed’ he meant, initially, partnerships of molecules that could store data and be programmed to carry out a sequence of operations. In the long run, the supramolecular assemblies should become capable of learning from their experiences. Indeed this was a key part of Lehn’s strategy. Inventing and synthesizing the necessary partnerships by conventional chemistry would take forever. Let natural processes do the work, as in the spontaneous, self-organized filling of the enzyme cleft.

His Darwinian evolution of molecules would lead on, Lehn believed, to Postdarwinian evolution in which the supramolecular partnerships would act like intelligent entities capable of literally shaping their own futures. Ultimately they could rival life itself. Lehn predicted: ‘Through progressive discovery, understanding, and implementation of the rules that govern the evolution from inanimate to animate matter and beyond, we will ultimately acquire the ability to create new forms of complex matter.’

In this staggering agenda, the opportunities for young researchers speak for themselves. As is often the case with new sciences, the rhetoric at first ran ahead of reality, but the rate of progress in the long run is likely be limited by the human imagination rather than by chemical feasibility. The transition from the 19th-Century partnerships of atoms in molecules, to the 21st-Century partnerships of molecules in supramolecular assemblies, will require a new mind-set. It may also bring chemistry out of its smelly back room.

The chemists who made huge contributions to science, technology, agriculture and medicine during the past 200 years were usually hidden like chefs, behind the feasts of physics, biology and industry. Their recipes, like those of the mathematicians, were written in a foreign language using strange symbols, discouraging to would-be fans. Terminology will be no simpler but the role of the chefs will be plainer, when they start sending out the dishes by molecular robots, fashioned from the commonplace atoms of the planet.

Any update for Magic Universe should emphasise the practical applications, drawing also on US-Spanish research published in 2009 (see the Lakhtakia reference). The addition shown here (which won’t be the last) probably fits best after the paragraphs about Manfred Sumper’s polyamine colouring of diatoms, and before the remarkable closing speculations of Jean-Marie Lehn.

Learning optical tricks from butterflies

Living organisms do other amazing things with colours. Butterfly wings get their shimmering patterns from molecular assemblies that inspire nanotechnologists. In 2010, Richard Prum and a multi-disciplinary team of colleagues at Yale discovered that cells growing on the surface of a wing fold themselves inwards in origami fashion to make intricate shapes called gyroids. Before the cells die, they coat the outer gyroids with starchy chitin, and the resulting crystals scatter light from a mulplicity of surfaces, giving colours that depend on the crystal dimensions, the incoming light and the angle of view.

Materials researchers at Penn State were already fascinated by the gyroids. They found ways to replicate them by dissolving away the chitin coats and gently depositing compounds based on germanium, selenium and antimony. Practical applications in nanotechnology were explored in collaboration with a team at the Universidad Autónoma de Madrid.

Coatings to improve the efficiency of photo-electric solar panels were among the possible early uses of the optical nano-structures. And as Raúl Martín-Palma of Madrid pointed out, butterfly wings were just a start.

“The technique can be used to replicate other biological structures, such as beetle shells or the compound eyes of flies, bees and wasps. … The development of miniature cameras and optical sensors based on these organs would make possible their installation in small spaces in cars, mobile telephones, and displays, apart from uses in areas such as medical endoscopes and security surveillance.”

References

Vinodkumar Saranathan, Chinedum Osuji, Simon Mochrie, Heeso Noh, Suresh Narayanan, Alec Sandy, Eric Dufresne and Richard Prum, “Structure, function, and self-assembly of single network gyroid (I4₁32) photonic crystals in butterfly wing scales,” Proceedings of the National Academy of Sciences, Vol. 107, No. 24, June 15, 2010.

Alan H. Schoen, “Infinite Periodic Minimal Surfaces Without Self-intersections.” NASA Tech. Note No. D-5541. Washington, DC, 1970. Available at http://ntrs.nasa.gov/archive/nasa/casi.ntrs.nasa.gov/19700020472_1970020472.pdf

N. Calder, Magic Universe, pp. 483-487, Oxford UP, 2003

Akhlesh Lakhtakia, Raúl J. Martín-Palma, Michael A. Motyka and Carlo G. Pantano. “Fabrication of free-standing replicas of fragile, laminar, chitinous biotemplates”. Bioinspiration & Biomimetics 4 (3): 034001, Sept 2009

Martin-Palma quote (lightly edited) is from http://www.physorg.com/news174223049.html which is based on a press release from FECYT, the Spanish Foundation for Science and Technology

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