Rewriting the Nitrogen Story: Plant cycles nutrient forward and backward

A study of a little yellow flower could add a new arrow to textbook drawings of the nitrogen cycle.

The horseshoe vetch (Hippocrepis comosa), a European relative of beans, is the first plant discovered to break down nitrogen-containing compounds in its tissues into a readily usable nitrate form, report Charles Hipkin of the University of Wales in Swansea and his colleagues. Textbook diagrams of the nitrogen cycle now show only microbes performing that task, Hipkin and his colleagues say in the July 1 Nature.

“This is the first paper I have seen that shows plants doing it,” says Josh Schimel of the University of California, Santa Barbara.

When Hipkin and his colleagues were surveying the nitrogen chemistry of legumes, they stumbled across hints that the horseshoe vetch was doing something odd. A series of experiments and surveys enabled the team to piece together the story.

In their shoots, the horseshoe vetch and some of its relatives build up high concentrations of a toxic, nitrogen-containing compound called 3-nitropropionic acid (3NPA). That toxin makes a handy defense against grazers, both mammalian and arthropod. When livestock eat plants laced with 3NPA, they become quite sick. In a lab experiment, Hipkin discovered that normally voracious locusts start trying to eat each other before they’ll take a nibble of leaves high in 3NPA.

Such a potent toxin could represent a risk to the organism deploying it. A damaged or elderly leaf could poison neighboring tissue as its compartments leak. So, Hipkin and his colleagues weren’t surprised to discover that the species they’ve found to have abundant 3NPA also show high activity of an enzyme that disarms the toxin. In that process, it creates nitrates and nitrites.

By collecting debris shed by horseshoe vetch, the researchers estimated that these plants were each year enriching the soil with at least 48 milligrams per square meter of nitrogen in usable form.

This vetch power gives a new tweak to nitrogen cycling. Nitrogen makes up some 79 percent of Earth’s atmosphere, but animals and plants can’t use nitrogen sniffed directly from the air. These organisms, including horseshoe vetch, get their usable nitrogen—ammonium and nitrates—either from nitrogen-fixing bacteria or from organic material broken down by microbes. By producing nitrates and nitrites directly, the vetch contributes usable nitrogen in a new way.

This activity might be widespread among legumes, says Hipkin. The more than 500 species tested so far contain 3NPA or a relative, a sign that these plants, too, may manage the breakdown chemistry. Legumes already have a special place in the nitrogen cycle because they typically house live-in colonies of the bacteria that convert nitrogen from the air into ammonium.

Schimel speculates that legumes’ direct breakdown of 3NPA won’t have huge ecological implications for most temperate ecosystems because it’s dwarfed by the microbial sources of nitrates. For certain ecosystems, however, the contributions might be greater.

“The system could be particularly important in dry ecosystems with soils extremely poor in nitrogen,” says Bernard Dreyfus of the Laboratory of Tropical and Mediterranean Symbionts in Montpellier, France.