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IN DEP TH

MICROBIOLOGY

Leaf bacteria fertilize trees, researchers claim By Elizabeth Pennisi, in Yosemite National Park, California

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he fastest growing trees outside the tropics are poplars. Tall and slender, they can reach 30 meters in less than a decade despite the seemingly inhospitable ground they favor—burned areas and sandy riverbanks, for example. Sharon Doty says the credit goes to microbes in their leaves and other tissues. While the poplar’s leaf cells are busy converting sunlight to energy, she says, bacteria between those cells are transforming nitrogen from the air into a form the tree needs to sustain this rapid growth. That’s a radical notion, because nitrogen fixation is generally thought to happen primarily in bacteria-rich nodules on the roots of legumes and a few other plants, and not in the treetops. “We are completely fighting dogma,” says Doty, a plant microbiologist at the University of Washington, Seattle. Earlier this month at the Fifth Annual Yosemite Symbiosis Workshop here, Doty bolstered her case. She reported the first direct evidence that poplars do get nitrogen from certain microbes, and she got support from Carolin Frank, an environmental microbiologist at the University of California (UC), Merced, who studies a different tree that thrives on poor soil. Frank reported that nitrogen fixation may also occur in the needles of limber 844

pines, which grow on stony, high-elevation slopes in western North America. Frank and Doty suspect that nitrogenfixing leaf bacteria may be widespread, and, if transferred to crops, could help boost yields on marginal soil. Doty has found that a number of crops grow better when inoculated with the bacteria, and at the Yosemite meeting she reported the latest to benefit: rice. Other plant biologists, although far from convinced, are paying attention. “If there’s an unrecognized set of nitrogen fixers in a wide number of [tree] species, that’s a big deal,” says Douglas Cook, a plant and microbial biologist at UC Davis. The belief that significant nitrogen fixation takes place only in those bacteria-filled root nodules has been under strain since the 1990s, when researchers discovered nitrogen fixing in sugarcane, which doesn’t have nodules. Since then, investigators have reported clues that bacteria called endophytes, which live inside plant tissues, provide nitrogen to their hosts. But, Cook contends, “the proper studies haven’t been done, and they are not trivial.” He and others argue that the nitrogenase enzyme key to the process is too sensitive to oxygen to work in leaves. And even if the microbes are processing nitrogen in the air, “that doesn’t mean that they are actually providing a host with any benefit,” says Sharon Long, a researcher who studies

nitrogen fixation at Stanford University in Palo Alto, California. Doty has tried to answer all of those objections. She first began to suspect that nitrogen fixation might take place outside root nodules about 15 years ago, when she discovered her poplar cell cultures were full of bacteria related to known nitrogen fixers. She put the bacteria on media that lacked nitrogen, yet some thrived—apparently getting their own nitrogen from the air. She’s since documented that dozens of bacterial strains from poplar promote growth not only of poplar but also of rye, turfgrass, maize, cottonwood, tomato, and now, she reported, rice. Her greenhouse experiments show that rice seedlings dipped for 4 hours in a broth containing poplar endophytes wind up with the microbes throughout the plant body and grow taller, have more biomass, and sprout more tillers—which produce heads of grain—than untreated rice. If Doty is right, a dose of the bacteria could be a boon to farmers. “Nitrogen is a huge constraint, particularly for farms in Africa,” says Katherine Kahn, a plant biologist and program officer at the Bill & Melinda Gates Foundation in Seattle. Current remedies fall short: Fertilizer is costly and environment-damaging, adding nitrogenfixing bacteria to the soil doesn’t work well, and equipping crops with the genes needed to form nodules or to fix nitrogen themsciencemag.org SCIENCE

22 MAY 2015 • VOL 348 ISSUE 6237

Published by AAAS

PHOTO: JEFFRY B. MITTON

Free-living nitrogen fixers defy textbooks and could boost crop production

NEWS

IMAGE: ESA

Growing in harsh conditions, limber pines may get help from nitrogen-fixing bacteria in their needles.

selves is still a distant dream. Skeptics note that some of the leafdwelling bacteria Doty has isolated make plant hormones, which could increase growth. But because Doty did these experiments in artificial soil lacking nitrogen, she argues that nitrogen supplied by the bacteria must be driving the growth. At the meeting, Doty’s former technician, Andrew Sher, reported what she considers the strongest evidence yet. Sher put cuttings from wild poplars into flasks and exposed them to a heavier form of nitrogen than exists in air. Afterward, the same isotope turned up in the plant tissues, evidence that the bacteria had captured it and converted it to a usable nutrient, Doty says. Frank converged on the same conclusion from a different starting point: a 2012 discovery that 30% to 80% of the microbes in limber pine needles were related to known nitrogen-fixing species. It struck her that these bacteria might explain a puzzle. In forests, foliage and soil contain more nitrogen than they should, given the known sources. Nitrogen-rich bedrock can explain some of the extra, but about 25% remains unaccounted for, says Benjamin Houlton, a global ecologist at UC Davis who specializes in the nitrogen cycle. “When you add up the numbers you come up short,” he says. If nitrogen fixers were at work in leaves and needles, they might balance the books, Frank thought. Still, she was initially skeptical. “I’d had a lot of doubt, lying awake at night,” she recalls. But at the meeting, she described putting a limber pine twig with needles into a jar and replacing some of the vessel’s air with acetylene. As microbes fix nitrogen, their nitrogenase enzymes convert acetylene into ethylene. The presence of ethylene at the end of the experiment told Frank that nitrogen-fixing microbes were at work, far from any root nodule. Others are now cautiously embracing the idea. “There’s a change in attitude, not from skepticism to believing but from skepticism to cautious questioning,” says Gerald Tuskan, a plant geneticist at Oak Ridge National Laboratory in Tennessee. Tuskan and his colleagues have isolated about 3000 microbes from poplar, many of which are equipped with nitrogenase. Some sequester themselves in biofilms with oxygen-limited compartments, where nitrogenase could function even in the leaf’s oxygen-rich environment. Bit by bit, the case for treetop nitrogen fixation is building, Frank says. “I think we are converting people slowly, including ourselves.” ■

EARTH SCIENCE

Alarm over a sinking delta Rise and Fall project seeks ways to slow land subsidence in Vietnam’s populous Mekong delta By Charlie Schmidt, in Soc Trang, Vietnam

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eaning over a pond carved into the soft soils of the Mekong River delta, Ngwyen Khuong strains to lift a net of flapping shrimp. “We can harvest 4000 kilograms from a pond like this every 3 months,” he says. But Khuong’s booming shrimp business may be undermining the very land it occupies. Shrimp farmers in the delta are pumping prodigious amounts of ground water into their brackish ponds, causing water tables to drop, overlying sediments to compact, and the land to subside. The trends could expose the world’s third largest river delta—home to some 20 million people—to flooding and other threats. “We face big problems if we have subsidence on one side and rising seas on the other,” says environmental scientist Nguyen Hieu Trung of Vietnam’s Can Tho University. An alliance of Vietnamese and Dutch scientists is now trying to get ahead of the problem. They met here recently to launch the Rise and Fall project, a $1 million, 5-year effort to better understand what’s driving Mekong delta subsidence and develop strategies to reverse it. “We know virtually nothing about what’s beneath our feet,” said geographer Philip Minderhoud, a co-leader of the project and doctoral candidate at Utrecht University in the Netherlands, dur-

ing the 11 March gathering. “In many places the rates, causes, and future implications of subsidence remain an open question.” Although researchers have documented subsidence in other large river deltas, they only recently published the first hard evidence that the Mekong delta, which covers some 55,000 square kilometers and sits about 2 meters above sea level, is sinking. Ground- and satellite-based instruments have clocked average subsidence rates of 1 to 4.7 centimeters per year, a group led by hydrogeologist Laura Erban of Stanford University in Palo Alto, California, reported last year in Environmental Research Letters. In Ca Mau, a province on the delta’s southern tip, the sinking reaches nearly 5 cm annually. Among the culprits: levees that prevent sediment from spilling out of rivers and into the delta, and some 1 million wells drilled since the 1980s for drinking and agriculture. If groundwater depletion continues at present rates, researchers estimate, the delta could sink by nearly a meter by midcentury. Ca Mau alone has more than 100,000 wells, which have caused water tables to fall some 5 meters and allowed seawater to creep inland, making the well water increasingly salty. At the meeting, the researchers began sharing what they know. The next step in the project, which is primarily funded by the Dutch Science Foundation, will be extensive

Subsidence threatens the Mekong delta’s rich farmland. Colors in this composite image reflect land cover changes over time.

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22 MAY 2015 • VOL 348 ISSUE 6237

Published by AAAS

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Microbiology. Leaf bacteria fertilize trees, researchers claim.

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