La crise du phosphore

Photo: ptrf.org

Notre monde sera à court d'un élément de base à la vie: le phosphore. Difficile à croire pour quelqu'un qui souffre à cause d'un surplus de phosphore dans la rivière devant chez elle. Mais voici l'explication scientifique de cette crise (une autre!).

Le phosphore est au coeur des avancées en agriculture et des problèmes environnementaux. Les biologistes commencent seulement aujourd'hui à comprendre l'importance du phosphore et le rôle qu'a joué et joue encore cet élément dans l'évolution et la santé humaine.

Voici l'histoire d'un limnologiste de Phoenix et un biologiste moléculaire à Atlanta qui travaillent tous les deux sur le dossier du phosphore. James Elser travaille au Arizona State University et étudie la vie aquatique dans les lacs et les cours d'eau. Il se passionne de l'évolution de la vie et s'inquiète des dommages causés par le surplus du phosphore sur nos écosystèmes, sans compter les répercussions que sa rareté graduelle aura sur nos vies à tous. George Beck est un biologiste moléculaire et cellulaire au School of Medicine du Emory University, où sa recherche se sert de souris en cage et des cellules humaines en culture. Quand il patauge dans un lac, c'est pour se baigner. Quand le phosphore l'inquiète, c'est parce qu'il pense à ses effets sur notre corps.

Le phosphore est un nutriment essentiel de la vie. Il est dans nos os, dans les membranes qui contiennent les cellules et leurs organelles, et est l'un des éléments de base de chaque molécule d'ADN et d'ARN, entre autres. La vie est impossible sans phosphate. Au travers de l'histoire de l'humanité, nous avons trouvé les phosphates dont nous avons besoin dans la viande et les produits laitiers, mais aujourd'hui, nous en absorbons trop en consommant trop de nourriture transformée qui contient des ingrédients ajoutés qui retiennent l'eau dans les viandes et les fromages, ainsi que les acides phosphorés dans les liqueurs douces.

Depuis l'apparition de la vie sur terre, la redistribution du phosphate disponible a façonné l'évolution, l'écologie et la physiologie. Dernièrement, par contre, le phosphate est la cause de problèmes de santé pour l'environnement et les humains. Les récoltes abondantes se réalisent grâce aux applications généreuses d'engrais qui contiennent des phosphates. Mais le ruissellement de sources agricoles intensives et des régions urbaines a provoqué des apparitions d'algues hors contrôle, suffoquant la vie des lacs et des cours d'eau. Étant un nutriment si essentiel, çà ne devrait pas nous surprendre que des doses trop généreuses pourraient aussi avoir des effets négatifs sur le corps humain. James Elser n'hésite pas à dire: "Le phosphate est l'accélérant biologique universel: ajouté aux systèmes écologiques et biologiques, tout va plus rapidement."

Jusqu'à ce que nous en manquions. Les humains utilisent plus de 150 tonnes de phosphate rocheux par année. Une scientifique environnementale du University of Technology, Dana Cordell, prévoit que la production de phosphate ne suffira plus à la demande d'ici 2033, et les réserves du globe seront épuisées d'ici 50 à 100 ans. Les mines où l'extraction est relativement aisée se font de plus en plus rares. Quand celles-là seront épuisées, nous devrons aller chercher le phosphore dans des gisements où le phosphore est contaminé par des éléments radioactifs comme l'uranium et le thorium, ou des métaux lourds comme le cadmium.

Pour y aller avec la pédale un peu plus doucement, les chercheurs comme Cordell suggèrent que nous devrions changer notre diète et améliorer nos usages de phosphates. C'est en étudiant des organismes aquatiques dans des lacs privés de phosphore qu'Elser comprend comment les organismes vivants s'adaptent au manque de phosphore disponible dans les écosystèmes. Son travail lui a permis de voir les liens entre la biogéochimie et l'écologie des lacs. Mais cela lui a fait réaliser des implications encore plus vaste: le phosphore, comme les autres éléments essentiels à la vie comme l'oxygène, le carbone, l'hydrogène et l'azote, pourrait être un facteur qui limiterait la croissance de la population humaine. Est-ce qu'un surplus de phosphore a aussi des effets comme sur les micro-organismes aquatiques qu'il a étudié? Un lien avec la santé humaine s'est révélé quelques années plus tard.

George Beck a grandi à Wilmington, au Delaware, près de la Baie de Chesapeake. Même à un tout jeune âge, il savait que les blooms d'algues étaient causées par le ruissellement des eaux qui contient le phosphate des engrais et des savons: "Le phosphate est vraiment le carburant de la croissance." dit-il du phénomène qu'il a observé maintes fois au niveau moléculaire.

Beck s'est intéressé au phosphate il y a environ 10 ans quand il s'est rendu compote que le composé chimique est plus qu'une base moléculaire. Il est un signal dans la génétique des cellules. Les signaux du phosphate déclenchent parfois des cancers dans des expériences in vitro. Il a passé les dernières 10 années à voir si cela était également vrai dans le corps d'une souris.

En laboratoire, ses souris ont été mises sur des diètes qui étaient soit déficientes, soit trop riches en phosphates. Elles furent exposées ensuite à un ingrédient cancérigène trouvé dans la fumée de cigarette. Bientôt, c'était évident que les souris qui consommaient trop de phosphates attrapaient le cancer beaucoup plus rapidement que les autres. Le scientifique de 43 ans n'est pas tout à fait prêt à dire au monde entier de changer sa façon de se nourrir, lui et son épouse ont déjà commencé: "Je travaille là-dessus depuis un bout de temps, et nous ne mangeons plus beaucoup de mets préparés maintenant. Certainement pas autant que l'Américain moyen."

Pourtant, nous savons déjà que le phosphate est la cause de la calcification des reins. C'est pourquoi les malades qui souffrent des problèmes de reins sont sur des diètes faibles en phosphate. Une autre étude récente, celle de Mohammed Razzaque, un biologiste cellulaire du Harvard School of Dental Medicine, a découver que les diètes à haute tenure de phosphate faisaient ager prématurément les souris, les rendant infertiles, réduisant le volume de leurs muscles et provoquant l'emphysème. Certains tissus du corps comme les poumons et l'aorte devenaient calcifiés, et la mortalité des cellules s'accélérait dans les reins, les poumons et les muscles: "Je crois que beaucoup de phosphate est physiquement toxique pour les cellules elles-mêmes, et cela a un effet cumulatif sur les organes du corps."

Extrait du sol, la roche qui contient du phosphate est transformée et ajouté aux savons, aux détergents, à l'herbicide de Monsanto RoundUp et dans les engrais. Aux États-Unis, le phosphate vient des mines en Floride, en Caroline du Nord et de l'Idaho, mais le pays devient de plus en plus dépendant du Maroc au fur à mesure que les mines se tarissent.

L'année dernière, l'écologiste Peter Vitousek de Stanford University et ses collègues ont écrit un commentaire dans la revue Science sur le débalancement des nutriments au travers le globe. Par exemple, les cultures de maïs au Kénya reçoivent 8 kilos d'engrais de phosphate par hectare par année, tandis qu'en Chine, les fermiers en épandent 10 fois plus, plus que les plantes peuvent absorber. Certaines recherches qui regardent la façon que les racines absorbent le phosphate ont découvert qu'il y a moyen d'aider les plantes à acidifer le sol, augmenter l'absorbtion du phosphate tout en doublant la biomasse du riz et des tomates, même dans des sols pauvres.

Des scientifiques tentent d'améliorer des récoltes par la génétique, d'autres essayent de récupérer le phosphate des eaux usées d'égouts et de ruissellement, d'autres tentent de mieux comprendre l'histoire naturelle du cycle du phosphore. Elser aime comparer le phosphore à l'or. "Nous avons un circuit fermé pour l'or. Après l'extraction dans la mine, nous fondons l'or et recyclons car l'or a de la valeur. Par contre, le phosphore s'écoule dans un seul sens dans nos écosystèmes." Seulement 20% du phosphate extrait du roc employé dans la production de la nourriture aboutirait dans nos corps. Le reste est perdu à cause de l'inéfficacité de la production d'engrais et l'épandage, ainsi que les méthodes de récoltes, la transformation et la distribution de la nourriture.

Mais dans les pays où le sol est pauvre, le phosphore est aussi précieux que l'or. Là, les plantes croissent lentement, les gens recyclent beaucoup et rien n'est gaspillé. Aussi, il n'y a presque pas de phosphore dans l'eau: il est emprisonné dans les organismes vivants qui font tout pour le garder. Dans des expériences scientifiques dans ces cours d'eau de ces pays-là, on a ajouté du phosphate dans certains cours d'eau: les limaces ont commencé à grossir, mais passé une certaine concentration, la croissance et la survie allaient en diminuant. Comme ce pourrait être le cas avec les humains, trop de phosphate dans la diète est néfaste.

On fait la connection avec les cancers chez les humains: parce que les tumeurs demandent beaucoup de ARN pour maintenir leur taux de croissance, on s'est douté que les tumeurs contenaient beaucoup de phosphore. Cela s'est avéré vrai: les tumeurs des poumons et du colon contiennent de 2 à 3 fois plus de phosphore que les tissus normaux, de même que du ARN. Mais le lien entre le phosphate et le cancer n'est pas toujours clair et net.

Pendant que la recherche continue, la bataille politique sur le phosphore commence juste à s'échauffer. Les industries d'additifs alimentaires et les compagnies de liqueurs douces questionnent les dernières études, et l'industrie du phosphate espère contre-balancer les pertes de ventes des détergents sans phosphates en accélérant la vente de batteries au lithium pour les autos qui contiennent du phosphate .

L'année dernière, Elser a fondé le "Sustainable P Initiative" au Arizona State University pour mettre le problème sous les projecteurs aux États-Unis (site ici: http://sustainablep.asu.edu/), et mène le symposium au American Geophysical Union à San Francisco en décembre: "Les choses se tassent, mais entre-temps, le phosphore nous coule entre les doigts."
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"ELEMENTAL SHORTAGE
The world is running out of cheap phosphorus, the element that lies at the heart of great agricultural advances and thorny environmental problems. Biologists are only now beginning to understand what it means for evolution and human health.

Although a limnologist in Phoenix and a molecular biologist in Atlanta have never met before, a single element ties them together. James Elser works at Arizona State University and studies aquatic life in lakes and streams. He has developed a fascination for the evolution of life from its earliest beginnings and worries about the damage an overabundance of phosphorus has done to our ecosystems and how its looming depletion will affect our lives. George Beck is a cell and molecular biologist at Emory University’s School of Medicine, where he pursues his research using caged mice and cultured human cells. The last time he stepped into a lake, he was just going for a swim. He thinks about biochemical pathways and signaling cascades. Yet he also worries about phosphorus. He worries about what it is doing to our bodies.

The element phosphorus, which naturally binds to four oxygen molecules in a variety of phosphate salts, is not just an essential nutrient—it is one of life’s fundamental nutrients. It is a component of bones, the phospholipid membranes that encircle cells and their organelles, the business end of the adenosine triphosphate (ATP) coenzyme that drives cellular machinery, and part of the backbone of every DNA and RNA molecule. Life, not to mention human life, is not possible without phosphate. Historically, humans have obtained phosphates from meat and dairy products but are ingesting more and more of it from processed foods, including moisture-retaining additives in meats and cheeses and the tangy phosphoric acids in sodas.From the time that life began on Earth, the global distribution of bioavailable phosphate has shaped evolution, ecology, and physiology. Recently, however, phosphate has also been causing environmental and human health problems. The Green Revolution of the mid-20th century owes its massive crop yields to the widespread application of phosphate fertilizers, but runoff from intensive agricultural practices and from urban areas has caused algae to grow out of control, suffocating life in lakes and other waterways. For such an essential nutrient, it should come as no surprise that high doses might also have negative effects on the human body. As James Elser puts it, “Phosphate is the universal biological accelerant: When you add it to ecological and biological systems, everything goes faster.”

At least until we run out. Humans use over 150 million tons of phosphate rock per year. In an influential paper last year, Dana Cordell, an environmental scientist at the University of Technology, Sydney, estimated that by 2033 phosphate production will no longer keep up with demand, and global reserves will be depleted within 50 to 100 years.1 Even if global supplies stretch for the next 300 to 400 years, as the phosphate industry contends, the most easily processed rocks are in ever-shorter supply, and the United States will have exhausted its reserves by 2050. When these reserves run out, the world will become more reliant on deposits that contain a lower concentration of phosphate and are laced with radioactive elements like uranium and thorium, or heavy metals like cadmium. “There is nothing on the market that can replace phosphate on the scale that we need it,” Cordell says.

To conserve phosphate, researchers like Cordell caution that we should change our diets and increase the efficiency with which we use phosphate. In other words: do exactly what some scientists believe our cellular pathways and unbalanced ecosystems are telling us we should be doing. Even though Elser, 51, had been studying phosphorus for his entire career, Cordell’s paper was the wake-up call he needed. Twenty-five years ago, the limnologist first headed out with a white-bearded desert rat and ichthyologist named Wendell Minckley to see the aquatic wonderland of Cuatro Ciénegas, not too far south of the Texas-Mexico border. The “four swamps” in this desert basin represent one of the world’s most unique and isolated ecosystems, with strange fishes and even stranger microbes. The Río Mesquites and surrounding ponds are crowded with mineralized microbial mats known as stromatolites. These mats once covered the Earth and are now generally known from just a few supersalty pools around the world, such as those in Shark’s Bay, Western Australia.Indeed, Cuatro Ciénegas has a venerable marine heritage—half its microorganisms trace their ancestry to an ancient ocean. But now it is freshwater, and this nutrient-deprived oasis is so starved for phosphorus that one bacterial species, Bacillus coahuilensis, has even opted for a sulfolipid membrane, rather than the ubiquitous phospholipid bilayer surrounding most other cells. In marine ecosystems, the ratio of carbon to phosphorus atoms in microbes is about 100:1. At Cuatro Ciénegas, it reaches as high as 5000:1.

Elser believes that studying these ratios, which are part of what he calls “biological stoichiometry,” is key to tracing not only the history of life but the workings of organisms and ecosystems. Years ago, he became enthralled by the fact that if you dump a bunch of phosphate in some lakes, tiny Daphnia quickly overtake their slower-growing microscopic crustacean neighbors, called copepods. What accounted for this difference in growth rates?

In the late 1990s, he sat down with a group of grad students and scribbled on a blackboard every biomolecule that contained phosphorus. He asked each member of the team to dig through the literature and find out which molecule commanded the most phosphorus in biological contexts. ATP is phosphorus-rich, but there is hardly any of it in the cell. Phospholipids are abundant, but not that high in phosphorus. DNA and RNA have the same amount of phosphorus per nucleotide, but there is between 2 and 20 times as much RNA in every cell. Growing organisms depend on a steady supply of RNA and, consequently, phosphorus. “We realized that there was enough extra RNA in Daphnia to explain all the extra phosphorus they have compared to copepods,” he says.

That work provided an early connection between biogeochemistry and lake ecology. But it also made Elser think about the wider implications, and the extent to which phosphorus—unlike common but crucial elements like oxygen, carbon, hydrogen, and nitrogen—might be the limiting factor in the expansion of the human population. Do humans respond to excess phosphate more like Daphnia or copepods? A link to human health would not reveal itself until several years later.

George Beck grew up in Wilmington, Delaware, a short drive from the Chesapeake Bay. Even at a young age, he knew about the huge algal blooms—fueled by runoff containing phosphate from fertilizers and detergents—that were smothering the copepods, crabs, and sea grass beneath them. “Phosphate really is a fuel for growth,” he says of the phenomenon he’s observed time and time again at a molecular level.

Phosphate sparked Beck’s scientific interest about 10 years ago, when he realized that the compound is more than just a molecular building block—it’s also an important signaling molecule. He was trying to figure out the molecular details of bone building. Surprisingly, the key turned out to be phosphate: An increase in free phosphate in the extracellular matrix around the bone-building osteoblast cells could directly change gene expression inside those cells, upregulating some pathways and downregulating others. Beck knew that phosphate-stimulated signaling pathways were not limited to osteoblasts. And when he began working at the National Cancer Institute in Bethesda, Maryland in 2000, he discovered that phosphate signaling triggered tumor growth in some in vitro experiments. If such a finding held up in a mouse model—a big if—it would suggest that excess phosphate consumption could lead to cancer. And that’s what Beck has spent the last 10 years trying to figure out.

In 2005, when Beck arrived at his new position on Emory’s Atlanta campus, he immediately began preparations for his first phosphate experiments with live mice, using a knockout strain that had been developed as a model for studying skin cancer. At 8 weeks of age, female mice were randomly assigned a diet of either 0.2 percent phosphate or 1.2 percent phosphate. In humans, the USDA recommends a daily phosphate intake of 1250 mg, although most Americans exceed that by about 100 mg. Beck’s mice were consuming the equivalent of either 500 mg or 1800 mg per day.

Beck then dosed the mice with a carcinogen from cigarette smoke called dimethylbenzanthracene, together with another chemical to stimulate cell growth, and examined them once a week for squamous cell carcinomas. It took just 12 weeks for 80 percent of the mice on the high-phosphate diet to exhibit skin papillomas, the initial stage of cancer. Mice on the low-phosphate diet didn’t cross the 80 percent threshold until 15 weeks later. More importantly, after 19 weeks, mice on the low-phosphate diet developed an average of six skin papillomas compared to 10 in the high-phosphate mice.

Although the 43-year-old scientist is not ready to tell the world to change its eating habits, he and his wife already have. “I’ve been doing this work for a while, and we don’t eat a lot of processed foods anymore—certainly not as much as the average American.”

Considered in a wider context, Beck’s finding was hardly an outlier. Phosphate has long been known to cause calcification of the kidneys, which is why patients with kidney disease are placed on low-phosphate diets. More recently, Mohammed Razzaque, a cell biologist at the Harvard School of Dental Medicine, has found that a high-phosphate diet in mice led to premature signs of aging, such as infertility, emphysema, and muscle wasting. Soft body tissues, including the lungs and aorta, became calcified, and cell death increased in the kidneys, lungs, and muscles. Although clinicians have often chosen to use the word “hyperphosphatemia” to refer to high levels of phosphate in the diet, Razzaque went with a more direct term in his paper: “phosphate toxicity.”

“I believe that high phosphate can be physically toxic to the cells themselves, and it will have a cumulative effect on the body’s organs,” he says.After being scraped from the ground, phosphate rock is processed from a chalky mineral into laundry detergents, Monsanto’s RoundUp weed killer, or fertilizer—its primary commercial form. The United States obtains most of its phosphate rock from domestic mines in Florida, North Carolina, and Idaho, but as those mines move toward exhaustion in the next 50 years, the country is increasingly dependent on Morocco, which sits atop the world’s largest phosphate reserves.

Last year, ecologist Peter Vitousek of Stanford University and colleagues wrote a commentary in Science pointing out the world’s great “nutrient imbalance.” Corn growers in western Kenya, for instance, apply just 8 kg of phosphate fertilizer per hectare per year. Compare that to China, where farmers are using more than 10 times that amount: 92 kg of phosphate per hectare per year—way more than what the plants can actually use. To solve this nutrient imbalance, some scientists have begun taking a closer look at how plants actually absorb phosphate through their roots. Roberto Gaxiola, a plant physiologist at Arizona State University, says that the key to boosting a crop’s phosphate-uptake efficiency is to enhance the transport of glucose produced by photosynthesizing leaves. “The roots are like you and me,” he says; “they don’t photosynthesize so they need the combustible carbon” from glucose. He’s found that upregulating an enzyme called proton pyrophosphatase in roots helps plants acidify the soil, absorb phosphate, and can ultimately double the biomass of rice, tomatoes, and Arabidopsis growing in phosphate-poor soil.

As physiologists like Gaxiola work to improve current crops through genetic engineering, and environmental engineers hunt for ways to recover phosphate from sewage and runoff in waterways, Elser and Beck believe breakthroughs could also come from a better understanding of the natural history of the phosphorus cycle. How does phosphorus move from organism to organism in ecosystems and what exactly does it do inside your cells? What mechanisms do organisms have to conserve it? Elser likes to compare phosphorus to gold. “We have a closed gold cycle,” he says; “after we mine it, we melt it down and recycle it because it is valuable. Phosphorus is on a one-way trip through our ecosystem.” According to Cordell’s analysis, just 20 percent of the phosphate rock used in food production makes it into our bodies. The rest is lost due to inefficiencies in fertilizer production and application, and crop harvesting, processing, and distribution.

At Cuatro Ciénegas, however, phosphorus is as precious as gold. “The creatures in Cuatro Ciénegas have been saving phosphorus for a long time,” says microbial ecologist Valeria Souza of the National Autonomous University of Mexico. “They grow slowly, they recycle a lot, and nothing goes to waste.” Souza has shown that there is practically no free phosphorus in the water: it is all sequestered away inside living organisms that fight mightily for it. “There is tremendous warfare to snatch the phosphorus from the dead,” Souza says. In fact, the dearth of phosphorus means that organisms in Cuatro Ciénegas have tiny genomes and are reluctant to swap genes through horizontal gene transfer—an isolating process that has ultimately led to their diversification. A pool 10 meters away will have a completely different biota, as Souza discovered by examining 16S rRNA genes from 350 cultivated strains of bacteria and archaea.

Soon after Beck began to recognize the importance of phosphate to osteoblasts in the early 2000s, Elser and his colleagues decided to find out what would happen if they added phosphate to streams at Cuatro Ciénegas. Immediately, the microbes coating the stromatolites in the streams took up the added phosphate and increased their rate of photosynthesis as well as their deposition of calcium carbonate. The snails that grazed on the microbial biofilms, in turn, grew faster and made more RNA, but only up to a point. As phosphate levels increased further, snail growth and survival declined. As may be the case in humans, excessive phosphate intake can be detrimental to snails.

In some sense, Elser’s study mimics an experiment that occurred on a global scale 520 million years ago during the Cambrian explosion, which resulted in a dramatic expansion in the diversity of life. Prior to the Cambrian, life on Earth looked a lot like Cuatro Ciénegas: dominated by stromatolites growing in shallow waters. Around 600 million years ago, fungi and algae began to colonize land and started to weather the geological formations where phosphate had been locked up since Earth’s formation. Indeed, around that time deposits of phosphorite, the geological term for phosphorous-rich rocks, begin to appear in the marine geologic record as organic material and weathered rock trickled into shallow seas. If the influx of phosphate could have triggered the Cambrian explosion—when life diversified into many of the phyla we still see today—then its depletion could well reverse it.Just as cancer biologists have begun to apply principles of evolution and ecology to understanding the dynamics of multiplying cell populations, Elser has begun to think about the stoichiometry of the human body. Because tumors require lots of RNA in order to maintain their high growth rate, Elser suspected that tumor cells were relatively higher in phosphorus.

In collaboration with John Nagy, a mathematical biologist at Scottsdale Community College, and other researchers, Elser analyzed the phosphorus content of primary tumors from the livers, kidneys, colons, and lungs of 121 patients. As predicted, lung and colon tumors had two to three times the phosphorus content of normal tissue, along with higher levels of RNA. However, the data for kidney and liver tumors did not support the theory, which led the team to posit that tumors in those tissues caused problems by having a lower cell-mortality rate, rather than a high cell-division rate, which would require more phosphate.

Told about Elser’s study, Beck perks up a bit. He was unaware of the theory, but says that it makes a lot of sense. “That’s my thinking,” he says. “Cells need more phosphate to proliferate.” In terms of early-stage cancer, the evidence is beginning to stack up. Along with Korean collaborators, Beck has found that a high-phosphate diet can double the risk of lung cancer in some mice. But the link between phosphate and cancer is far from clear. In a separate study by the Korean group, phosphate can also suppress lung cancer. Meanwhile, a French group, led by Laurent Beck of the Université Paris Descartes, has recently found that knocking out a sodium-phosphate transporter in cultured cells can decrease cell proliferation and tumor growth.

As research presses on, the political battle over phosphorus is just starting to heat up. The International Food Additive Council and the British Soft Drinks Association have challenged the recent work on dietary phosphate by Beck, Razzaque, and others, while the phosphate industry hopes to counter a decline in laundry detergent sales with an uptick in the use of phosphate in lithium-ion batteries for electric vehicles. Dana Cordell complains that the international community has yet to establish agreements to study the issue, as they have with topics such as carbon-dioxide emissions or nitrogen pollution from fertilizer.

Last year, Elser founded the Sustainable P Initiative at Arizona State University to raise the profile of the problem in the United States, and is leading a symposium at the American Geophysical Union in San Francisco this December. “It’s all coming full circle,” he says. The phosphorus, however, keeps trickling away."

Excerpts from article written by Brendan Borrell published in The Faculty of 1000 here:
http://www.the-scientist.com/article/display/57777/

Meanwhile, I would sure appreciate it if corn fields kept it to themselves, as the water treatment plants. Maybe then I could go back swimming in my river again!