eat light: dawn of the plantimals

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32 | NewScientist | 11 December 2010

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Page 1: Eat light: Dawn of the plantimals

32 | NewScientist | 11 December 2010

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Page 2: Eat light: Dawn of the plantimals

11 December 2010 | NewScientist | 33

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Could a fish with built-in photosynthetic bacteria help feed the world, ask Debora MacKenzie and Michael Le Page

Dawn of the

plantimalsIT WAS a long shot,” says Christina Agapakis.

“We just wondered what would happen.” She has done an extraordinary experiment:

injecting photosynthetic bacteria into the eggs of zebrafish.

Agapakis, a research student at Harvard Medical School in Boston, only wanted to see if the bacteria could survive. Bacteria that get into larger cells usually kill or are killed, but occasionally things work out differently, with consequences that can transform the planet. The ability to turn light into food evolved in cyanobacteria, and plants evolved when more sophisticated cells stole the technology by enslaving cyanobacteria within themselves.

While most biologists would have bet that cyanobacteria and fish do not mix, the Synechococcus that Agapakis injected into the eggs were still alive two weeks after the fish hatched, which is the point when the pigment of zebrafish develops. The bacteria might survive longer in a transparent strain.

However, the cyanobacteria did not grow and divide as normal. They also didn’t provide much sugar to the fish, says Agapakis, so the fish embryos got little if any energy from light. This was true even for cyanobacteria genetically modified to export sugar. Yet the mere fact that both fish and cyanobacteria survived raises tantalising questions. Could we one day create fish that get part of their energy from sunlight? Could photosynthetic animals help feed the world?

of the developing salamander embryos. Inside the salamander cells, energy-burning mitochondria cluster around the algal cells as if to gobble sugar and oxygen, Kerney announced earlier this year.

We don’t yet know for sure that the salamander embryos get food from the algae, and it seems unlikely this happens in adult salamanders, which spend the day hiding under moss or stones, and whose mostly black skin would not let much light through anyway. Nevertheless, it appears at least one vertebrate is partly photosynthetic during a brief period of its life cycle.

The question, then, is not whether animals can photosynthesise, but why relatively few do. Some researchers think for most animals, the downsides of photosynthesis usually outweigh the benefits. Others disagree. “I think the answer is not that they can’t, just that they haven’t,” says Patrick Keeling of the University of British Columbia in Vancouver, Canada, who studies chloroplast evolution. To get a better idea of who is right, we need to look at what it takes to photosynthesise.

Where there be LightThe first requirement is light. It is surely no coincidence that animals in which photosynthesis has evolved already had lifestyles that involved staying in the light, and that many, like hydras and jellyfish, also have translucent bodies that let light through.

Body shape also matters. Plenty of photosynthetic animals, such as anemones and corals, have a branching structure similar to that of plants. Others, including flatworms and some sacoglossan sea slugs (pictured overleaf), have a flat, leaf-like shape. This gives these creatures a large surface area relative to volume, maximising the amount of light – and thus energy – that can be captured.

The need for light might explain why many animals do not photosynthesise. Even if adult spotted salamanders could get a little energy from photosynthesis, for instance, the risks of exposing themselves during daytime probably outweigh any benefit, meaning this ability will never evolve further. And while many mammals, birds and reptiles get plenty of light, their fur, feathers or scales prevent the light reaching living cells.

Then again, it seems even a little light will do. The nudibranch sea slug Plakobranchus ocellatus must benefit from photosynthesis even though it spends its day half-buried in sand and its photosynthetic cells are >

COVer StOry

“ This might sound laughable, but lots of animals already get part of their food from photosynthesis. The best known are the tropical corals, but many sponges, anemones, sea squirts, hydras and bivalves also rely partly on solar energy. In fact, solar-powered animals already help feed us, in a small way; giant clams have been part of the human diet for at least 100,000 years.

If you are thinking all these animals look and behave rather like plants, that’s not always the case. There are plenty of free-living photosynthetic animals. Photosynthetic flatworms up to 15 millimetres long can be found in huge numbers in places. Then there are the jellyfish-like Vellela, which float on the sea surface, and the upside-down jellyfish. Most striking of all are the many different kinds of solar-powered sea slugs.

As yet, the list doesn’t include any vertebrates – but that might be about to change. It has long been known that algae grow in the jelly surrounding the eggs of some amphibians. Both sides benefit: the algae supply oxygen and eat the embryos’ waste.

Now it turns out that the spotted salamander Ambystoma maculatum goes even further. Ryan Kerney of Dalhousie University in Halifax, Canada, has discovered that females store algal cells in their oviducts and somehow pass them on to their eggs. Even more amazingly, the algae do not just grow on the outside of the eggs but also within the cells

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Page 3: Eat light: Dawn of the plantimals

shaded by flaps of skin. Nor is a flat or branched body the only way to get it. The silica skeletons of some sponges act like fibre-optic cables, channeling light to cells deep within them.

Perhaps the most unlikely photosynthesisers are the giant clams, with their thick shells and relatively small surface area. Despite this, a young clam can keeping growing for 10 months powered by light alone. To achieve this, giant clams have undergone major internal rearrangements, says Angela Douglas of the Bermuda Institute of Ocean Sciences. However, these extensive adaptations would not have evolved if photosynthesis had not benefited clams right from the start.

In fact, photosynthetic algae have even been found inside the bodies of some small bivalves, conchs and snails, apparently thriving on the low levels of light that penetrate the shell. It is thought the hosts are gaining some food from the algae, though it hasn’t been proven.

If clams and conchs can get enough light for photosynthesis, surely some fish could too? Indeed, some fish, like lionfish and leafy sea dragons, or rays and flatfish, seem to have ideal shapes for capturing light.

Transmuting sunbeamsThe second requirement for photosynthesis is the machinery for turning light into food. In plants, this comes in the form of chloroplasts, stripped-down descendants of the cyanobacteria that were engulfed by the ancestors of plants around 2.5 billion years ago. The ancestors of animals never had chloroplasts, but one kind of animal can acquire them.

Solar-powered sacoglossan sea slugs extract chloroplasts from the algae they feed on and tuck them away inside gut cells. Branches of the sea slugs’ gut extend throughout their bodies, providing a large surface area for capturing light.

But there is a catch. As cyanobacteria turned into chloroplasts, most of their genes moved to the genome of the host, including some essential for keeping chloroplasts working. Since sea slug cells do not have these genes, they must replace their chloroplasts every few days or weeks. The exception is the emerald green Elysia chlorotica (pictured). After it steals the chloroplasts from one particular alga upon reaching its adult form, it doesn’t need to eat again for the remaining 10 months of its life.

Has E. chlorotica somehow acquired the genes needed to keep chloroplasts working? Yes, two teams announced last year, but they might have been too hasty. Mary Rumpho of the University of Maine in Orono, who heads one of the teams, has been unable to confirm the finding. “The final verdict awaits sequencing of the genome,” she says.

To sustain chloroplasts requires 200 or so extra genes, she says, and adding them to

an animal’s genome would be an enormous challenge for today’s genetic engineers. “It is unrealistic to think you could insert all the nuclear genes needed to sustain chloroplast activity in a foreign genome, and get them expressed, and the protein products targeted to the chloroplast, not to mention regulating the genes’ activity,” says Rumpho.

This would explain why the many organisms that have stolen the ability to photosynthesise from plants have usually done so by enslaving entire cells – nucleus, chloroplasts and all (see diagram, opposite). Adding an entire plant cell to an animal cell would require less genetic tinkering than adding only chloroplasts. The obvious candidate is the alga Symbiodinium, which provides the solar power in corals, anemones, jellyfish, nudibranch sea slugs, giant clams and other animals. The other option is to add cyanobacteria to animal cells, as Agapakis did – some sponges and corals already play host to cyanobacteria.

Even if vertebrates tolerate algae or cyanobacteria within their cells, though, it wouldn’t be enough. “Coral polyps somehow induce Symbiodinium to release the sugar it makes,” says Douglas. “Outside the polyp, it keeps that sugar for itself, thanks very much.”

Such inducement is not the only challenge. While the single-celled amoeba Paulinella chromatophora has acquired a cyanobacterial endosymbiont that is losing genes and turning into a chloroplast, in a repeat of the ancient event that gave rise to plants,

no multicellular organism has acquired the ability to pass a photosynthetic endosymbiont down the generations like this. “Incorporating a chloroplast into a multicellular organism is very different from a unicellular one,” says Chris Lane of the University of Rhode Island in Kingston, who studies endosymbiosis. “Getting it passed on, controlling the cell division cycle, is not trivial.”

Animals that do not pass down photosynthetic endosymbionts within eggs have to acquire them from the environment and distribute them around their body. Photosynthesis might have evolved multiple times in sea slugs in part because they can already extract toxins and stinging cells from their prey and distribute them around their body, but this is a very rare talent.

No free lunchA photosynthetic lifestyle really is like a day at the beach: you can get too much sun. “It would be kind of nice to be a photosynthetic animal and use sunlight when food was scarce,” says Rumpho. “But you also have to develop ways to withstand the damage caused by absorbing high energy from sunlight.”

Damaging ultraviolet light is also a big problem, as is heat for those that live on land. Animals that stayed in the blazing sun all day would have problems staying cool, which might be partly why all known photosynthetic animals are aquatic.

Then there is the cost of producing and

34 | NewScientist | 11 December 2010

Elysia chlorotica steals the ability to turn light into food from algae

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maintaining photosynthetic machinery, not to mention the anatomical compromises needed to carry the tools for both photosynthesis and eating. Photosynthetic anemones, for instance, often have both long, stinging tentacles to capture prey, and short, algae-loaded ones to capture sunlight. They use their hunting tentacles only at night.

What does all this tell us? While there does not appear to be any fundamental obstacle to animals photosynthesising, it is very hard for most animals to acquire the necessary machinery. What’s more, many animals would need major changes in lifestyle and anatomy to benefit even if they did somehow acquire the machinery, and the intermediate stages would decrease their chances of survival, so it is hard to see how it could ever evolve.

Genetic engineering might be able achieve what evolution hasn’t, but would the benefits outweigh the costs for any vertebrates, especially energy-hungry animals with active lifestyles? Let’s say we have induced Symbiodinium to live in the skin cells of a fish the way it lives in coral polyps. Coral fixes 3 to 80 grams of carbon per square metre of photosynthetic surface per day, according

to Stuart Sundin of the Scripps Institute of Oceanography in La Jolla, California. In energy terms, that is 126 to 3360 kilojoules.

The surface area of a typically shaped 20-gram fish, including fins, is 0.0044 m2 or so; for a 500 g fish it is 0.045 m2. According to fish nutritionist Ingrid Lupatsch of Swansea University in the UK, a 20-gram carp, ready for stocking in an aquaculture pond, needs about 3 kJ a day to maintain its weight; a harvestable 500 g fish needs 40 kJ.

Do the sums and you find that – in theory – photosynthesis could supply carp with several times the energy they need for maintenance. This makes photosynthetic fish look like huge winners, and similar back-of-the-envelope calculations suggest that even energy-guzzling mammals could get a useful amount of energy from light – but there are huge “buts”.

For starters, genetically engineered fish are unlikely to be anywhere near as efficient as corals honed by millions of years of evolution. There are a whole host of changes required. To maximise their exposure to light, for instance, fish would have behave differently. They need clear skin and scales to let light through to cells, but protection from UV light. And, like corals, solar-powered fish might thrive only in the tropics, where there is lots of sunlight, clear water and steady temperatures.

In addition, what most photosynthetic animals get from their symbionts is a fast fix of carbohydrates that Douglas calls “junk food”. Proteins, vitamins and minerals all come from eating. Too much sugar can be bad for fish, and, in the case of fish farming, carbs are cheap to provide. The costly part is providing protein and oils; most carnivorous fish, such as salmon, have to be fed fishmeal. In theory, equipping fish with modern nitrogen-fixing cyanobacteria, as found in some sponges and corals, would enable them to make as much protein as they need, but nobody’s managed to do this in plants yet despite decades of effort.

In any case, some farmed fish like carp and tilapia already get part or all of their food from plants growing in their ponds, and animals that feed on these plants. Sticking the algae inside the fish might not be any better.

The surprising answer then, is that it might well be possible to create solar-powered fish, but that such fish might not provide any clear advantage when it comes to food production. And without that, no one will invest in creating them, especially given the need to convince regulators and consumers that they are safe. But if genetic technology continues to advance in leaps and bounds, someone’s sure to carry on where Agapakis left off. Maybe one day feeding your pet fish will be as easy as turning on the light. n

Debora MacKenzie is New Scientist ’s Brussels correspondent. Michael Le Page is the biology features editor

11 December 2010 | NewScientist | 35

Stolen technologyAnimals like corals owe their ability to photosynthesise to a long history of piracy

Simple cells called cyanobacteria evolved the ability to photosynthesise2.5 billion years ago

A complex cell enslaved the cyanobacteria, which evolved into the chloroplasts found in plants and algae

CYANOBACTERIA

CHLOROPLAST

PLANTS

FLAGELLUM

ANIMAL CELL

NUCLEUS

Another cell enslaved an entire algal cell, giving rise to dino�agellate algae

DINOFLAGELLATE

Corals, anemones, nudibranch sea slugs and other animals play host to a dino�agellate called Symbiodinium

NUCLEUS

” The algae grow within the cells of salamanders, and appear to supply them with food and oxygen”

NIC

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LAS

E. C

URT

IS A

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RAY

MA

RTIN

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