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Border between Egypt (left) and Gaza and (right). The difference in the shades of the terrain in the uncultivated areas reflects changes in the soil on the Egyptian side. This makes this border one of the few that can be seen from space.

Max Planck Research · 1 | 2021 FOCUS

ALGAL BLOOM IN THE DESERT SAND

TEXT: KLAUS WILHELM

29 PHOTO: SCIENCE PHOTO LIBRARY/PLANETOBSERVER PHOTO SCIENCE PHOTO:

Drought, heat, and glaring sun. A desert habitat is one of punishing extremes. If a plant is to survive here, it must be able to endure a . This is especially true for algae. Together with Mark Stitt and his team at the Max Planck Institute of Molecular Plant Physiology in Golm near Potsdam, Haim Treves is investigating how the alga Chlorella ohadii has adapted to the extreme living conditions of the desert.

Max Planck Research · 1 | 2021 FOCUS

“At first, we thought our measuring devices were Chlorella ohadii is a unicellular green alga that is named after the man who discovered it, the eminent biochem- malfunctioning. But it ist and photosynthesis researcher, Itzhak Ohad. He was Treves’ long-time mentor and friend, who died in wasn’t the instruments – it 2016. Ohad was the first to isolate and study this orga- nism, and his research made a major contribution to was the algae.” our fundamental understanding of photosynthesis. It has now been 10 years since Haim Treves was a PhD student at the Hebrew University in Jerusalem, where HAIM TREVES he regularly explored the desert. The young scientist brought back samples from his excursions to the Israeli Negev Desert of the wafer-thin sand crust that covers “blue-green algae”, many of which perform photosyn- the desert’s floor. “This crust has the consistency of thesis and get their energy from sunlight. Treves and cornflakes in the areas of the Negev that are farther his colleagues wanted to isolate these bacteria from the away from the coast. It breaks with a soft crackle when sand crust and grow them in the laboratory. But tiny you step on it. But along the coast, where the air is more green specks would always appear in their cell cultures humid, it feels more like you’re stepping on a sponge,” after a short time. “At first, we thought we had been describes Treves. careless and contaminated our samples,” he recounts. But they just couldn’t get rid of the green specks. The crust appears completely lifeless. But in fact, it har- Itzhak Ohad finally persuaded Treves to look into the bors a unique community of microorganisms. For mystery. Treves identified the green specks as colonies example, cyanobacteria – bacteria formerly known as of the green algae Chlorella ohadii. “I really owe him a

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Cyanobacteria of the genus Leptolyngbya form unbranched chains. They are found in a wide variety of habitats, e.g. in thermal springs, in , as well as in . In the Negev Desert, the cyanobacteria live in the crust that covers the ground. PHOTO: CCALA PHOTO:

Max Planck Research · 1 | 2021 PHOTOS: HAIM TREVES/MPI OF MOLECULAR PLANT PHYSIOLOGY Border between Israel (foreground) Israel Border between In Egypt. and Chlorella Chlorella algae The green Desert, while the Egyptian side, in contrast, is largely largely is side, contrast, in Egyptian the while Desert, result of the destruction of the soil crust by vehicles crust of soil the of destruction result the a is devoid –this sand covered is and in of vegetation ohadii and overgrazing. spring, flowers bloom on the Israeli side of Negev Israeli the bloom on the flowers spring, drates, which can store water which can drates, SUMMARY crops to enable them to to enable them crops employs various adaptations adaptations various employs even levels at high of solar out. Bacteria form agel-like form out. Bacteria Researchers want to transfer want to transfer Researchers photosynthesize effectively – – effectively photosynthesize layer by carbohy excreting to protect its photosynthetic photosynthetic its protect to this alga’s properties to to alga’s properties this sand. than better and solar radiation in the the in radiation solar and radiation. soil of the Negev Desert. It of Negev Desert. the soil surface protects it from drying it drying from protects surface soil on the thick millimeters only few Acrust sunlight. glaring the against mechanisms defies extreme drought extreme defies

ohadii Even at light the four intensity times the of desert, the light shone researchers the on it, faster the it grew. the alga’sthe abilities: not only extraordinary did tion, and it me makes lives very happy legacy his that on in the name of this alga.” of name the this on in Treves quickly recognized algae continued to flourish. “We continuedalgae to flourish. thought it our was special debt and inspira of forspecial gratitude guidance his

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defy to more sunlight –the extreme exposure was notwas due but to instruments, rather the Mark Stitt was also fascinated by dis the fascinated also StittMark was Stitt. Treves it So that only was logical Planck Institute of Molecular Plant Phys leave familiar territory.leave familiar we If focusing are how differently adapt plants to their can known. “But it’s sometimes idea agood to fault our meters and that were defective,” growing organisms ever discovered. organisms growing conditions that plants can developconditions plants can that com covery. The former at Max the Director colleagues, he uses model organisms such model he uses organisms colleagues, pletely capabilities,” unexpected says environment. And it’s under extreme tats on Earth – it one of also is fastest the on Earth tats toes, and tomatoes because the genetic the andbecause tomatoes toes, technology to cutting-edge iology uses on only afew to it overlook easy species, is to to research photosynthesis.research Like most of his material of these plants has been decoded, been plants of has these material and many of metabolic their pathways are as as says Treves. However, this phenomenon Treves. phenomenon says However, this survives in one in ofsurvives most the extreme habi Chlorella ohadii itself: not only it does ohadii Chlorella Arabidopsis thaliana Max PlanckResearch , spinach, pota- spinach, , FOCUS Chlorella Chlorella ·1 | 2021 - - - - -

The life of this alga is characterized by extremes: during characterized is The alga life of this Particularly the photosynthesis of this alga is optimally optimally is photosynthesis alga the Particularly of this Beyond a certain point, increased solar radiation no lon radiation solar point, increased Beyond acertain produced carbohydrates that have combined with the sand sand the have with combined that produced carbohydrates “singlet oxygen” – a highly reactive form of oxygen that crust stores water better than pure sand and it protects the the it and protects pure sand than water stores better crust Chlorella Chlorella and baked into a brittle crust resembling cornflakes. This This cornflakes. resembling crust into abrittle baked and Dryness intensifies this effect, because it the hampers because effect, this intensifies Dryness little oflittle one much and too of other. the hydrogen atoms. However, sun’s the rays strong too are up and heat completely sun to the 60°C; out dry the damages the photosynthetic apparatus. photosynthetic the damages ground. The proper amount of water and light that got his doctorate, got he so his could research conduct further ger leads to ahigher leads ger photosynthetic output. it Instead, overloadedgets and melts down – like ashort circuit,” portant role into converting portant energy in chemical solar before too justperiod sunrise, once there is after again form. At can plummet frost dawn, little the that far so explains Stitt.explains High light produce also intensity can machinery photosynthetic the “Then desert. the in to ‘splitenergy it water’ into oxygen and turn and provide electrons state.energy energized These the energy. For every photon absorbed is by that chlo the the day,the it not is for to uncommon to rise temperatures on on rophyll molecules, one elevated is electron into ahigher moisture that there is in the air settles as dew as on the settles air the in there is that moisture adapted to such conditions. play Electrons im- an soil. At night, can on other the temperatures hand, should Planck he after to Max Golm go Institute the in stagnates and even decreases with increasing radiation. radiation. increasing with and even decreases stagnates Chlorella ohadii. Chlorella A layer about two millimeters thick covers the desert desert covers the thick A layer about millimeters two surface. Over many decades, microorganisms have microorganisms decades, Over many surface. needs to available is needs exist only brief the in ground from erosion and complete and erosion from desiccation. ground - -

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M

An electron microscope reveals the details of the P photosynthesis mechanisms of Chlorella ohadii. The chloroplast occupies a large part of the cell. Its stacked membranes (M) make photosynthesis particularly effective. The pyrenoid (P) serves the

same purpose. It is PHOTO: HAIM TREVES/MPI MOLECULAR OF PLANT PHYSIOLOGY enriched with the carbon dioxide needed for photosynthesis as well as a key enzyme. The pyrenoid is surrounded by a layer of starch (light ring).

500 nm

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use of the light energy to drive carbon dioxide fixation produce 60 times more starch than under low levels of and other metabolic reactions. The researchers found light. “The growth rate of the algae increases within that Chlorella ohadii has evolved several mechanisms – minutes – it’s like a turbocharger gets turned on,” says some unique – as protection against such short-circuits. Treves. They allow the alga to quickly establish a balance between oxidation and reduction reactions. Without But all these adaptations would not be enough if there this balance, too many electrons would accumulate. were not another very special habitat in the Negev De- “Like a car that shifts into a lower gear when going sert that, together with bacteria and fungi, enables the down a steep hill, this alga prevents damage to the algae to survive under the most adverse conditions: the photosynthetic system,” says Haim Treves. Further- two-millimeter-thick crust on the desert floor. It is more, the electrons flow within a closed circuit during photosynthesis in Chlorella, because only a circulatory system can prevent a surplus of energy-rich electrons under the desert’s extreme conditions. Otherwise, the electrons would be stuck like cars in a traffic jam, with some even flowing backwards. Chlorella also produces “Plants often develop enzymes that neutralize destructive singlet oxygen molecules. unexpected abilities, Studies by the Max Planck researchers also revealed that especially under Chlorella can effectively photosynthesize even in low light. The alga employs the very same ‘tricks’ when it extreme conditions.” grows in low light that it uses to cope with very high light intensities. When solar radiation increases, Chlo- rella can quickly raise its photosynthetic output and MARK STITT

Max Planck Research · 1 | 2021 FOCUS

ADAPTATIONS TO LIFE IN THE DESERT

ROOTING formed when the pioneers of the de- Formation of deep or In general, bacteria seem to be the sert – the cyanobacteria – settle on extensive roots secret rulers of this ecosystem. If the surface of the sand layer. Over resources become exceptionally many years, they produce large scarce, the bacteria can even bring the amounts of carbohydrates, which SAVE WATER growth of the algae completely to a Impermeable surface (e.g., a form a gel-like mass. This mixes with layer of wax) halt. the sand grains and creates a crust when it dries. The gel can better Closed stomata during the day The importance of the ecological retain the moisture when water in the Fewer or smaller stomata function this soil crust performs is form of dew or – very rarely – rain visible along the Israeli-Egyptian bor- wets the soil. It also dries out more Smaller or no leaves der. Tire tracks and other signs of slowly than pure sand. This allows Hair as protection against human activity dominate the Egyp- the crust to provide more water for light and evaporation tian side. Because the crust is largely the microorganisms living within it. destroyed, a sandy desert has spread Only when over half of the stored out on this side of the border. The water has evaporated over the course SUN PROTECTION Israeli Negev on the other side is a of the day do the microbes tempora- C4-photosynthesis: restricted military area and may not Nocturnal CO2 fixation in the rily cease their activity. In laboratory form of malate and the be entered by unauthorized personnel. experiments, Treves was able to conversion to carbohydrates So there the crust is still largely intact. demonstrate that the crust actually during the day The significance of this becomes evi- 33 prevents its community of microbes dent after rare rainshowers in the de- from drying out: together, cyanobac- Production sert: the Egyptian Negev remains teria and Chlorella survive the aridity of sun protection factors, brown, but the Israeli Negev blossoms like aloe typical of the desert – on their own, and briefly transforms into a sea of the algae would die. Researchers have Minimizing the area flowers. “The crust prevents the sand even found evidence that this exposed to the sun from spreading. So plants can thrive crust-dwelling organisms prepare for by turning away from there after it rains,” explains Treves. daily desiccation: before sunrise, the the light cells produce substances that will The Chinese government has reco- help them revive from their dry state DISTRIBUTION gnized the crust’s stabilizing on sand the following night. “Dormant” seeds that and soil fertility. In an experi- take years to germinate ment, Chinese researchers have ino- in drought conditions culated sand dunes of the Hopq De- Tiny tubes sert with cyanobacteria and artificially Explosive growth irrigated them. They’re hoping a sand in the crust of seedlings in the presence of moisture crust and ultimately arable soil will be created in this way. It remains to be Treves’s mentor Itzhak Ohad and his seen whether such measures will be colleagues have observed other fasci- successful. Treves takes a different nating phenomena under the micro- approach to helping crops grow better scope. The cyanobacteria can form vertical tubes in in arid and semi-arid . In his opinion, Chlorella which they can migrate towards the light. “When we ohadii itself is the key: “If we understand what makes it put a piece of crust in a Petri dish in the lab and spray so resistant to drought and high levels of sunlight and water on it, the bacteria come to the surface and form a how it can grow so quickly, we can provide other plants green layer upon it. Other times, the crust seems to with the same capabilities,” says Treves. Perhaps this turn black, because the bacteria are shielding them- tiny green algae holds one of the keys to sustaining life selves with endogenous sun protection factors,” says as global warming continues. It would not be the first Treves. Chlorella and the other microorganisms in the time that a presumed measurement error turned out in crust also benefit from this light protection. Thus, retrospect to be an important scientific discovery. without the cyanobacteria, the algae could not survive. www.mpg.de/podcasts/extreme (in German)

Max Planck Research · 1 | 2021