The Monthly Fern—More Quirks of Quillworts

Jon Keeley with several of his beloved quillworts (date unknown).

Once again The Monthly Fern series is featuring the Prairie Quillwort and its relatives—genus Isoetes. One post was not enough for these fascinating plants! Not only are they the sole survivors of a plant group that dominated 300 million years ago (see last month's post), they use CAM photosynthesis (1) ... that's astonishing! In fact it's so unexpected that when Jon Keeley announced it 40+ years ago, he was written off as ignorant (Keeley 2014).

Here's the conundrum. CAM photosynthesis is thought to have evolved in flowering plants (angiosperms) in hot arid environments. Many succulents, including most cacti, are CAM plants. But quillworts are primitive spore-producing lycophytes predating flowering plants by c. 200 million years. And almost all are aquatic.

Isoetes and other lycophytes split from ferns and seed plants long ago (source; black, red labels added).

Lycophyte diversity by Kingfiser (click link for full names and more info).

When I was an undergraduate long ago, only one type of photosynthesis was known (or so we were taught). As a grad student a decade later, I learned there were three: C3 is the common type; C4 and CAM are restricted to certain groups and situations (2). Since then I've largely ignored photosynthesis. But when I read that quillworts are CAM plants, I was intrigued! It was time to learn more. (Information here is from Khan Academy's Biology Unit 8, Photosynthesis unless noted otherwise.)

Photosynthesis: 1st stage powered by sunlight; 2nd makes food & oxygen for us to consume.

Photosynthesis is complicated and very chemical, but the basic process is simple. There are two stages. In the first, energy from sunlight is captured and converted to chemical energy. In the second, this chemical energy is used to convert carbon dioxide and water into glucose and similar carbon-based compounds, releasing oxygen in the process.

These are the benefits we reap. We consume carbon-based compounds for energy and to build proteins, DNA, muscles and more. And we breathe oxygen. If photosynthesis were to stop, we would die—either starve or suffocate.

As wonderful as photosynthesis is, there's room for improvement. The widespread C3 type, used by 85% of plants, is surprisingly inefficient. Carbon dioxide is captured and a sugar molecule created only about 65–80% of the time. The problem lies with an important but indiscriminate enzyme—rubisco—which will happily bind oxygen instead of carbon dioxide if given the chance (more here). 

Rubisco is the "molecular equivalent of a good friend with a bad habit" (KA, modified slightly).

This inefficiency is significantly less in C4 and CAM photosynthesis. But there's another problem and it's a big one—water loss. Plants take in carbon dioxide from air via stomata (pores) on leaf surfaces. But water vapor is lost at the same time, especially on hot dry days. Many plants close their stomata at night to prevent water loss, and when it's hot, some close stomata during the day as well. But then there's no source of carbon.

This is where CAM plants excel. They open their stomata at night and collect carbon dioxide, storing it for use the next day when the sun is shining. That way they can photosynthesize without opening their stomata and losing water. So clever!!

CAM photosynthesis requires extra energy compared to the common C3 type, but apparently it's worth the cost. CAM is used by at least 16,000 species, c. 7% of all plants. Most are desert plants, including at least 99% of the 1700 species of cacti (source). And then there are the quillworts, nearly all of which are aquatic at least part of their lives. Why would they bother with energy-expensive CAM?

Isoetes melanopoda, Prairie Quillwort, uses CAM even though it's aquatic (©2015 Robbin Moran).

Prairie Quillworts photosynthesizing by the light of day, with CO2 they gathered before dawn (Andrey Zharkikh).

Like terrestrial CAM plants, aquatic quillworts gather and store carbon dioxide at night but for a different reason. Terrestrial CAM plants have no access to CO2 during the day because their stomata are closed to prevent water loss. Quillworts have no risk of water loss, but for them daytime uptake of CO2 is difficult. It diffuses poorly in water to begin with, and most of the other plants in the pond are better at sucking it up for photosynthesis (4).

By the end of the day, the amount of CO2 in pond water is quite low. But as soon as night falls and photosynthesis stops, it quickly rises. "This must be when quillworts open their stomata to collect CO2" you may be thinking—as I did. But then a memory floated to the surface. Stomata don't work underwater! Aquatic quillworts have none, or non-functional ones at most.

From what I've read, there's still much to be learned about carbon dioxide uptake in Isoetes. However we do know that it varies with species and habitat. The few quillworts that are fully terrestrial—never submerged in water—have functional stomata and use C3 photosynthesis. They never use CAM, nor can they be converted to CAM even by keeping them underwater for a long time.

Isoetes histrix, Land Quillwort, is terrestrial (but often reported as aquatic). Late season photo by Sam Thomas; added insert by Peter de Lange.

Those quillworts that live part of their lives submerged, for example in vernal pools, are impressively versatile. They utilize CAM until water is low enough to expose their leaf tips to air. Then the stomata start to become functional and C3 photosynthesis begins to take over, progressing down each leaf cell by cell keeping just above the water! (Keeley 2014)

Isoetes howellii in dried vernal pool. It was in Howell's Quillwort that Jon Keeley stumbled upon CAM photosynthesis. © 2004 Carol W. Witham.

The many quillworts that are entirely aquatic are more puzzling. They have no stomata and their leaves are covered with a waxy cuticle. And yet they thrive, especially where other plants can't.

Aquatic Isoetes lacustris, the Lake Quillwort (Alina Ambrosova).

Isoetes lacustris in its favorite environment—lake bottom with sparse vegetation (5). (Alina Ambrosova) 

Aquatic quillworts seem to be more common in oligotrophic waters, where nutrients are scarce and there's little competing vegetation. So how do they survive if other plants can't? Probably with their unusual roots (6).

These roots have a large central air cavity that accumulates carbon dioxide gathered from sediments. Next to the cavity is bundle of vascular tissue that delivers it to the plant above. Furthermore, being CAM plants they collect CO2 at night as well as during the day, thereby doubling their harvest. Sometimes they truly flourish, covering the lake bottom in a dense green underwater carpet! (Moran 2004)

And with that, I will close. As you may suspect, this was one of my more challenging posts. Just when I had everything figured out, another puzzle would present itself. But I'm not complaining. In fact that's what I enjoy most about getting to know plants—pondering and unraveling their many little mysteries. And I know that the next time I meet up with a quillwort, it will be far richer experience.

So primitive, so simple in form, and yet so alluring (Isoetes englemannii, Nathan Aaron).

Notes

(1) C2 carbon concentration is sometimes considered a type of photosyntheses.

(2) CAM refers to crassulacean acid metabolism. To be clear, there is no "crassulacean acid"; the name refers to acid metabolism in the family Crassulaceae, where CAM was discovered (source).

(3) The widespread occurrence of CAM likely is due to repeated convergent evolution. After sequencing the pineapple genome, Ming et al. (2015) concluded that CAM arose from relatively simple reconfiguration of C3 pathways. See also Wickell et al. 2021.

(4) Many aquatic plants collect CO2 via bicarbonate; it appears that quillworts are unable to do this (Keeley 2014).

(5) Is that an alga on the leaves of Isoetes lacustris? If so, it might affect light capture but not CO2 uptake, which is done by the roots.

(6) Isoetes lacustris roots look very much like the fossilized roots of Lepidodendron trees, its ancient relatives.

Sources (in addition to links in post)

Keeley, JE. 1981. Diurnal acid metabolism in vernal pool Isoetes. Madroño 28:167-171. BHL

Keeley, JE. 1998. CAM Photosynthesis in submerged aquatic plants. The Botanical Review 64:122–158. PDF.

Keeley, JE. 2014. Aquatic CAM photosynthesis: A brief history of its discovery. Aquatic Botany 118: 38–44. http://dx.doi.org/10.1016/j.aquabot.2014.05.010

Lane, N. 2010. Life Ascending: The Ten Great Inventions of Evolution. WW Norton & Co.

Moran, Robbin. 2004. "Some Quirks of Quillworts" in A Natural History of Ferns. Timber Press.

Wickell, D, et al. 2021. Underwater CAM photosynthesis elucidated by Isoetes genome. Nat Commun. 12:6348 (open access).

Photosynthesis to the Rescue?

Every morning when the sun rises, millions of plants go to work converting solar energy to chemical energy, which they then use in the course of their lives for metabolism, growth, flowering, and so forth. We use it too, for we eat plants. So do our livestock, before we eat them. Even our fossil fuels started as photosynthesizing plants, as did plastics, and wood of course. Plants power the world, through clean renewable energy made from cheap abundant ingredients: water and carbon dioxide.

On a hot summer day in Kansas, millions of tiny chloroplast factories (upper right) are converting water and carbon dioxide into life-giving sugars and oxygen (source and source).

If plants can produce abundant cheap clean renewable energy, surely we clever humans can too. Bill Gates thinks so, as does the World Economic Forum (1). So do dozens of research groups currently working on artificial photosynthesis (AP):

“The benefits of artificial photosynthesis are numerous and include increased energy independence and efficient means of storing and dispatching of solar energy. Supporting the development of the foundational science and core technologies required for solar-fuel generation is the first step toward an investment in a future sustainable energy industry.” Joint Center for Artificial Photosynthesis

Artificial photosynthesis mimics photosynthesis in plants in a non-biological setting. Researchers are making good progress, but it probably will be at least a decade before you can buy an AP reactor.

Artificial photosynthesis in proposed twin-reactor system (Lee et al. 2013, modified)—not on Amazon just yet.

Photosynthesis is complex, but for this post, only the two basic steps are relevant: water splitting and carbon fixation. First water is split into hydrogen and oxygen, with oxygen released to the atmosphere. Next the hydrogen moves to the carbon fixation step. Atmospheric carbon dioxide is split, and carbon is combined with the hydrogen to make sugars, where energy is stored as chemical bonds. The sugars are broken down in respiration—providing energy for metabolism, growth, flowering, etc.—and carbon dioxide is released back into the atmosphere. The amount released is the same as that taken up in photosynthesis, so the overall process is carbon-neutral, and therefore “clean” (2) (3).

Basics of photosynthesis (source, modified).

Natural photosynthesis needs major tweaking to produce replacements for our fossil fuels. Sugars won’t do. And plants are inefficient at converting sunlight to chemical energy—only 0.1 to 8.0%, depending on temperature, type of light, and amount of carbon dioxide available. In contrast, mass-produced solar panels are 6 to 20% efficient. Researchers are addressing these limitations, and progress has accelerated recently thanks to new nano-scale methods and advanced materials.

Water splitting was achieved relatively early, and now is being improved in terms of cost, efficiency and durability. But the second basic step, carbon fixation, has taken much longer to replicate in the lab. Carbon dioxide must be split, and it’s an extremely stable compound. That’s why it accumulates in the atmosphere instead of breaking down. (Even if we were to switch completely to clean energy, the carbon dioxide already in the atmosphere won’t go away without active removal.)

Until recently, artificial carbon fixation produced only useless soups of 1-carbon compounds. But things have changed. With nanotechnology, AP components now can be designed down to the level of atoms, providing fine-scale control over function. Within the last two years, multiple labs have been able to split carbon dioxide to produce multi-carbon compounds in pure form (e.g. Kim et al. 2017).

How to make copper catalysts that fix carbon better than anything found in nature! (Kim et al. 2017, modified).

We now know that artificial photosynthesis will work, but continued research is needed to improve performance, reduce costs, figure how how to build suitable reactors, and more. Even if AP emerges successfully from research, it still has to cross the aptly-named Valley of Death, where many new technologies die before reaching commercial viability.

Traditionally governments fund research. Venture capitalists inhabit the Valley of Death, investing in high-risk projects in the hopes that at least a few will be high-yield.

New breakthrough technologies like AP are referred to as “blue sky” research—too early to know which will succeed in the real world. So if we are going to expand and diversify our energy portfolio, and make the transition to 100% renewables, we must invest in many blue sky candidates. And we must do it soon, because it usually takes decades for new technology to be widely deployed.

“But why bother?” you ask. “We’re already transitioning to renewables—solar and wind.” You’re absolutely right. Renewables are increasing fast. But they aren’t keeping up with growth in energy demand. “Despite decades of progress, about 80% of the world’s energy still comes from fossil fuels—the same as in the 1970s” (Rathi 2017). Even worse, today’s renewables are inadequate to make a full transition away from fossil fuels. The biggest challenge is in manufacturing, which contributes 20% of global emissions. Heavy load transport (shipping, aviation, land freight), which contributes 10% of emissions, also is out of reach of today’s renewables, due battery limitations (4).

“But is technology the only solution?” That question came up repeatedly in Energy Security, a terrific class offered by the International Studies Department, University of Wyoming (5). Whenever someone suggested conservation instead of technology, I flashed back on the late 60s and early 70s when Baby Boomers were conserving energy to save the planet. We even agreed to drive just 55 mph on the highways. Now we’re mega-consumers, contributing to fossil fuel’s relentless growth. Fossil fuels make for a wonderful life, and humans are not inclined to give them up, even those who agree that the amount of carbon dioxide (a greenhouse gas) being added to the atmosphere will warm the climate enough to destabilize the world on a grand scale.

It seems we must switch to renewable energy, not just to avoid climate change, but also to deal with the inevitable dwindling supply of fossil fuels. To do this, we need new innovative technologies … soon.

“The world has made remarkable progress in wind and solar over the past decade, and these technologies will continue to play an important role in our zero-carbon energy mix. … But because the scale of the challenge of providing reliable and affordable power without contributing to climate change is so vast, and the future energy needs are so great, we need to explore as many viable solutions as possible.” – Bill Gates, 2016

Source.

Notes

(1) Gates considers artificial photosynthesis to be one of three breakthrough technologies “that could solve the energy problem.” The Breakthrough Energy Ventures fund selected AP as one of seven innovation challenges, and the World Economic Forum and Scientific American included it on the list of “Top 10 Emerging Technologies of 2017.”

(2) “Clean” does not mean that photosynthesis is carbon-free, nor it does it necessarily remove carbon dioxide from the atmosphere on a net basis. Photosynthesis is sometimes mistakenly referred to as carbon-negative, probably because forests are widely recognized as Negative Emissions Technology (NET). Trees sequester carbon for hundreds of years (or longer if used for building materials) before death and decomposition return release it. Therefore on a human timescale, trees remove carbon from the atmosphere.

(3) Technically fossil fuels are carbon-neutral, for they originate as sugars produced through photosynthesis. Anaerobic fermentation of accumulated dead plant tissue produced the hydrocarbons we burn as fuel, releasing carbon “back” into the atmosphere. However, millions of years are required to produce hydrocarbons, much too slow to take up the carbon released in burning them. On a human timescale, the net effect is increased atmospheric carbon dioxide.

(4) Elon Musk of Tesla has challenged the view that current battery technology is unsuitable for large-scale applications. On November 16, 2017, he unveiled a prototype of an electric semi-truck able to travel 500 miles between charges at $1.26 per mile, compared with $1.51 for diesel. Skeptics immediately questioned his claims, but advance orders are coming in, starting with Walmart (15 trucks). Two weeks later, Tesla installed a battery at a wind farm in the state of South Australia, expected to power 30,000 homes. These batteries are immense. The semi-truck battery underlies the entire cab; the wind farm battery is the size of an American football field. It will be some time before either can be evaluated—at least a year for the trucks.

(5) I took advantage of UW’s policy of free courses for senior citizens. My final paper was about innovation in renewable energy, with artificial photosynthesis as a case study.

Sources

Bourzac, K. 2016 (November 21). “Will the Artificial Leaf Sprout?” Chemical and Engineering News. https://cen.acs.org/articles/94/i46/artificial-leaf-sprout-combat-climate.html (accessed September 30, 2017).

Gates, B. 2016b (December 12). “A New Model for Investing in Energy Innovation.” Gatesnotes. https://www.gatesnotes.com/Energy/Breakthrough-Energy-Ventures (accessed December 1, 2017).

IRENA. 2017a. “Accelerating the Energy Transition through Innovation.” International Renewable Energy Agency. http://www.irena.org/publications/2017/Jun/Accelerating-the-Energy-Transition-through-Innovation (accessed October 30, 2017).

Kim, D., et al. 2017. “Copper Nanoparticle Ensembles for Selective Electroreduction of CO2 to C2–C3 Products.” PNAS 114: 10560-10565.

Rathi, A. 2017 (December 4). “Humanity’s Fight against Climate Change is Failing. One Technology can Change that.” Quartz. https://qz.com/1144298/humanitys-fight-against-climate-change-is-failing-one-technology-can-change-that/ (accessed December 15, 2017).