Photonics research clams up

One of the first things you do when you are an adorable giant-clam larva floating in sun-blasted shallows around the western Pacific or the Red Sea is to capture and store within your tiny Tridacnidae self a couple of the Symbiodinium algal cells floating throughout your habitat. You may be no larger than a dust speck, but you now have the symbiotic partners you need to drop to the ocean bed, find a good place to stick yourself, and grow into a giant clam. You could end up living longer than a century, spanning four feet in length, and weighing as much as 500 pounds.

That's plenty of molluscan wow to ensnare a marine biologist's attention, but it's the giant clams' voluptuous blue and purple iridescent lips that Alison Sweeney, a professor of physics and of ecology and evolutionary biology at Yale University, could not resist. That was close to a decade ago when, as a postdoc at the University of California, Santa Barbara (UCSB), she went to Palau, an archipelago in Micronesia, to study iridescence in sea creatures.

Since then, she and other giant clam biologists have helped unveil just how elegant natural photonics technology can get and how, in the case of giant clam/algae symbioses, it appears to be central to the performance of one of the most efficient photosynthetic systems on the planet. What's more, as the biologists have been teasing out more of the clams' biophotonic wonders, engineering-minded collaborators have been adapting lessons from the clam biophotonics to high-tech applications, among them solar cells and optical wireless communication.

Scientists want to know more about giant clam iridocyte cells and their natural ability to manipulate light.  Credit: S. Rossbach

Sweeney is happy her work is inspiring technology developers, but it's the light-mediated symbiosis of the clams and their algal partners that widens her eyes the most. She thinks of the giant clams as algae farmers. As a clam larva matures into an adult and giant status (when it's the size of praying hands), it domesticates photosynthetic Symbiodinium cells on industrial scales. "It grows the one or two or three algae cells it scoops up early on into this dense monoculture array within its skin," Sweeney says. "It grows the algae cells at much higher densities than otherwise would happen for the algae [in the open ocean]. And the clam takes care of them just like a farmer by building a biophotonic infrastructure that provides them with a goldilocks amount of light to make photosynthesis run at an optimum rate and efficiency."

Biophysicist Amanda Holt, a Yale colleague of Sweeney's, calculates that mature giant clams harbor some 100 million algal cells per cubic centimeter of mantle tissue, which is the often brilliantly colorful tissue lining the clam's two fluted shell halves. These algae reside in pillared arrangements—like dense rows of soybeans, Sweeney points out—that penetrate several millimeters into the mantle. At those depths, the algae shouldn't be able to efficiently photosynthesize. They shouldn't be able to produce the glycerol, glucose, and other molecules the clam needs to live—unless there is some way of shunting sunlight arriving at the mantle surface to even the deepest algal cells.

This is where the clam biophotonics story comes in. In a 2014 paper in the Journal of the Royal Society Interface, Sweeny, her USCB research supervisor, Dan Morse, Holt, and colleagues from NASA Ames Research Center and the University of Pennsylvania (U. Penn.) described how the star of the biophotonics show is a cleverly organized population of light-manipulating cells known as iridocytes. The same type of cell that confers iridescence in squid dye, they reside in the top millimeter or so of giant clam mantle tissue. "It is a solar panel that, instead of making electricity, makes energy rich molecules by shunting sunlight to hundreds of millions of symbiotic algal cells," Sweeney says.

Also found in squid, octopus, hatchetfish, and other sea creatures, iridocytes are loaded with stacked layers of photon-engaging proteins. Like Bragg filters made of a grid of tightly spaced lines, these stacked layers do wonders with light. Using light-measuring probes that Holt developed in her garage, the researchers managed to gather and measure the intensity and wavelengths of light at different depths of mantle tissue. The researchers observed that the iridocytes scatter photosynthetically productive light sideways and downward such that it illuminates the entire length of the algal pillars. Meanwhile, the Bragg-mirror structures dominating each iridocyte's volume back-reflects otherwise damaging ultraviolet (UV) light away from the clam and algal symbionts. That's also where the alluring lip colors come from.

Iridocyte cells mediate photonic cooperation between giant clams and their photosynthetic symbionts. Credit: Imaging and Characterization Core Lab, KAUST.

Using a double-probe technique, they have measured photosynthetic efficiency at varying depths in the clams' tissue. One probe flashes controllable wavelengths and intensities of blue light into the algal pillars, while the other probe measures light that emerges from the same hyperlocal neighborhoods of tissue. In this protocol, Sweeney explains, "the more red fluorescence there is, the more the light is going to nonphotosynthetic pathways. The less fluorescence there is, the more efficient is the photosynthesis." Sweeney has been stunned by just how little red light emerges. As she sees it, the dimness of this red output could mean the photosynthesis of the clam/algae tag team is as good as any photosynthesis happening anywhere on the planet.

Ecologist Susann Rossbach, working with colleagues at the King Abdullah University of Science and Technology (KAUST) in Saudi Arabia, also took a deep dive into giant clam iridocytes. With poetic flare, in a paper published last year in Frontiers of Marine Science, they describe the iridocytes as mediating "photonic cooperation between giant clams and their photosynthetic symbionts."

Rossbach points out where she thinks her team has added to the biophotonics story Sweeney and her colleagues already have uncovered: "Our observations indicate that, in addition to the backscattering of nonproductive wavelengths, iridocytes of giant clams are also able to absorb ultraviolet radiation and re-emit it, shifted toward longer wavelengths." Those re-emissions, Rossbach suggests, in turn can drive up photosynthesis in the algal symbiont cells yet more.

The KAUST group's work began in earnest on 29 August 2018, when Rossbach and coworker Silvia Arossa collected two giant clams on the Abu Shosha reef in the Red Sea, which is not far from the KAUST campus. Sweeney started her work with a pair of clams that she harvested herself. The team then made absorbance and photoluminescence measurements by shining excitatory pulses of light into successive paper-thin regions of mantle tissue and measuring the spectrum of light that emerged. The researchers observed spectral shifts of the 325-nm stimulus light toward less dangerous and potentially more photosynthetically useful wavelengths ranging between 365 and 550 nm.

Sweeney and Holt note that there are many molecules in giant clam tissue capable of causing spectral shifts. As such, they caution that the spectral shifts Rossbach's team has observed do not necessarily mean they play a specific biological role of contributing to the photosynthetic efficiency of Symbiodinium cells.

Regardless of the uncertainty, Sweeney and Rossbach concur that the algal symbionts' photosynthetic efficiency would be impossible without the photonic assistance of the iridocytes. Same goes for the photonic protection against damaging and photosynthesis-thwarting UV radiation (UVR). These benefits, among others, are what enable giant clams to thrive in relatively shallow water where UVR would otherwise be debilitating, Rossbach says.

Probing yet further into the basis of the iridocytes' photonic traits, the KAUST group zeroed in on the signature multilayered stacks within the iridocyte cells. Previous research has indicated that these stacks are made of platelets of protein and crystallized guanine (one of DNA's four nucleotide bases) alternating with sheets of cytoplasm. Based on spectral-shift measurement with pure crystallized guanine, the KAUST team argues that the intracellular guanine crystals serve as the basis of the "photonic cooperation between the bivalve host and their photosynthetic symbionts."

Although the full account of the biophotonic properties underlying the symbiosis of Tridacnidae clams and Symbiodinium algae is yet to be revealed, the story in hand already has compelled engineering-minded investigators to steal what they can in pursuit of new technologies.

Under a recently completed US National Science Foundation (NSF) Inspire Award, which supports interdisciplinary collaborations, Sweeney joined forces with U. Penn materials scientist Shu Yang. With an eye on emulating clam iridocytes' ability to forward-scatter sunlight, Yang's lab synthesized artificial iridocytes as a means of redistributing light energy on micrometer and millimeter scales. Their specific tack was to synthesize nanoscale silica particles and pack them into gelatin microspheres.

The artificial iridocytes "show wavelength selectivity, depending on the size of the nanoparticles, had little loss, and a narrow forward-scattering cone, similar to that seen in giant clams," Sweeney and Shu write in a report to NSF. They add, "The Yang lab created a variety of bioinspired microparticles utilizing energy-downhill mechanisms seen in cells and assembled light-responsive nanoparticles that demonstrated photothermal effect and solar transparency, which could potentially be applied to improve solar-cell performance." The duo also outline the potential of using the synthetic iridocyte structures, and their tunable photonics properties, to tailor the transparency and thermal insulation of windows.

In parallel, Rossbach and her biology colleagues at KAUST teamed with technology developers in the university's photonics laboratory who took a stab at applying giant clam biophotonic manipulations to the cause of optical wireless communication. Reporting in Optical Materials Express, the researchers peg their interest on the intensifying need for high-capacity optical communication links as the Internet of Things undergoes explosive growth. The iridocytes' natural ability to manipulate light, including UV wavelengths, is tantalizing to the researchers because the higher- frequency light can accommodate high-bandwidth optical communications and data transfer.

In the same paper, an interdisciplinary team of 14 KAUST researchers, including Rossbach but led by Boon Ooi of the photonics laboratory and biologist Carlos Duarte, report a series of optical measurements using iridocytes embedded in mantle tissue of Red Sea giant clams. Based on the data, they say, iridocytes could be used "as a high-speed color converter for mid-deep UV photodetection, well-suited to application in mid-deep UV optical wireless communication."

Giant clam mantle tissue. Credit: S. Rossbach

The iridocytes' biologically useful property of down-converting ultraviolet solar photons to lower-frequency photons could point a way toward clam-inspired optical components, Ooi and his team say. The iridocytes, or artificial photonic structures based on them, could both detect high-frequency ultraviolet signals and then convert them into visible wavelengths for which silicon photodetectors are especially responsive. So, the Ooi team says, combining iridocyte-inspired UV photodetection with silicon-based optical components could provide a novel approach to designing optical communication systems for Internet-of-Things devices, among them wearable health monitors and wireless inventory trackers.

A key finding by the Kaust team was that the iridocytes have short photoluminescence decay times of about a nanosecond. That, in turn, enabled the team to show that the cells can modulate light from UV LEDs with a 22 MHz bandwidth, which Rossbach explains could translate into data-transmission rates of tens of megabits per second.

"Our colleagues are now trying to either extract pure iridocytes from the mantle tissue or artificially synthesize such materials, which would be a first step toward an optimization strategy," says Rossbach, who recently became environmental chemical science manager with the Red Sea Development Co.

Pleased as she is by the possibility that the evolving story of giant clam biophotonics could lead to new technologies, Sweeney says she is most wowed by how the more she and her scientific partners learn about the clam's photosymbiotic system, the more efficient the algal photosynthesis seems to be.

"Clams are way better than soybeans. They are even better than Iowa corn, and that is saying a lot. They are on par with spruce forests, which are very efficient," Sweeney says. "As far as we can tell," Sweeney says of giant clam mantle, "this small bit of tissue might be the most photosynthetically productive ecosystem on Earth."

Ivan Amato is a writer, podcaster, and crystal photomicrographer based in Hyattsville, Maryland.