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

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, Lotus japonicus, with rhizobia bearing nitrogen fixation or
nitrogen metabolism knockouts, and factorially varied molecular sources of
nitrogen fertilizer. Lotus 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 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.