Nitrogen fertilization nullifies host sanctions against non-fixing rhizobia and drives divestment from symbiosis in <i>Lotus japonicus</i>

Plants and animals house microbes that provide critical nutrients, but little is known about host control over microbial cooperation when resources are also accessed from the environment. Changes in nutrient access can challenge the host's ability to detect and selectively reward beneficial partners, destabilizing symbiosis. Legumes acquire nitrogen from soil and from symbiosis with rhizobia, but it is unclear if extrinsic sources of nitrogen interfere with host control systems. We inoculated the legume <i>Lotus japonicus</i> with rhizobia-bearing nitrogen fixation or nitrogen metabolism knockouts, and factorially varied molecular sources of nitrogen fertilizer. <i>Lotus</i> hosts selectively rewarded beneficial rhizobia and sanctioned non-fixing strains when extrinsic nitrogen was unavailable. Host benefits were undiminished when inoculated with rhizobia-bearing nitrogen metabolism knockouts, suggesting redundancies in nitrogen provisioning systems. However, under nitrogen fertilization, hosts did not discriminate between fixing and non-fixing rhizobia. Fertilized hosts formed miniaturized nodules housing limited rhizobia, divesting from symbiosis. Thus, sanctioning mechanisms rely on the detection of nitrogen fixation differences among rhizobia strains and can break down in nitrogen-rich environments. Nonetheless, divestment from symbiosis offers legumes robust host control, minimizing investment into rhizobia strains, irrespective of their capacity to provide benefit, when symbiosis services are not needed.