Nonnodulating Bradyrhizobium spp. Modulate the Benefits of Legume-Rhizobium Mutualism.
Rhizobia are best known for nodulating legume roots and fixing atmospheric nitrogen for the host in exchange for photosynthates. However, the majority of the diverse strains of rhizobia do not form nodules on legumes, often because they lack key loci that are needed to induce nodulation. Nonnodulating rhizobia are robust heterotrophs that can persist in bulk soil, thrive in the rhizosphere, or colonize roots as endophytes, but their role in the legume-rhizobium mutualism remains unclear. Here, we investigated the effects of nonnodulating strains on the native Acmispon-Bradyrhizobium mutualism. To examine the effects on both host performance and symbiont fitness, we performed clonal inoculations of diverse nonnodulating Bradyrhizobium strains on Acmispon strigosus hosts and also coinoculated hosts with mixtures of sympatric nodulating and nonnodulating strains. In isolation, nonnodulating Bradyrhizobium strains did not affect plant performance. In most cases, coinoculation of nodulating and nonnodulating strains reduced host performance compared to that of hosts inoculated with only a symbiotic strain. However, coinoculation increased host performance only under one extreme experimental treatment. Nearly all estimates of nodulating strain fitness were reduced in the presence of nonnodulating strains. We discovered that nonnodulating strains were consistently capable of coinfecting legume nodules in the presence of nodulating strains but that the fitness effects of coinfection for hosts and symbionts were negligible. Our data suggest that nonnodulating strains most often attenuate the Acmispon-Bradyrhizobium mutualism and that this occurs via competitive interactions at the root-soil interface as opposed to in planta



Rhizobia are soil bacteria best known for their capacity to form root nodules on legume plants and enhance plant growth through nitrogen fixation. Yet, most rhizobia in soil do not have this capacity, and their effects on this symbiosis are poorly understood. We investigated the effects of diverse nonnodulating rhizobia on a native legume-rhizobium symbiosis. Nonnodulating strains did not affect plant growth in isolation. However, compared to inoculations with symbiotic rhizobia, coinoculations of symbiotic and nonnodulating strains often reduced plant and symbiont fitness. Coinoculation increased host performance only under one extreme treatment. Nonnodulating strains also invaded nodule interiors in the presence of nodulating strains, but this did not affect the fitness of either partner. Our data suggest that nonnodulating strains may be important competitors at the root-soil interface and that their capacity to attenuate this symbiosis should be considered in efforts to use rhizobia as biofertilizers.
Department of Plant Pathology and Microbiology, University of California, Riverside, Riverside, California, USA Department of Biology, University of California, Riverside, Riverside, California, USA.
Kelsey A
KA
Gano-Cohen
Department of Biology, University of California, Riverside, Riverside, California, USA.
Peter J
PJ
Stokes
Department of Biology, University of California, Riverside, Riverside, California, USA.
Mia A
MA
Blanton
Department of Biology, University of California, Riverside, Riverside, California, USA Department of Botany and Plant Sciences, University of California, Riverside, Riverside, California, USA.
Camille E
CE
Wendlandt
Department of Biology, University of California, Riverside, Riverside, California, USA.
Amanda C
AC
Hollowell
Department of Biology, University of California, Riverside, Riverside, California, USA.
John U
JU
Regus
Department of Biology, University of California, Riverside, Riverside, California, USA.
Deborah
D
Kim
Department of Biology, University of California, Riverside, Riverside, California, USA.
Seema
S
Patel
Department of Biology, University of California, Riverside, Riverside, California, USA.
Victor J
VJ
Pahua
Department of Biology, University of California, Riverside, Riverside, California, USA Department of Botany and Plant Sciences, University of California, Riverside, Riverside, California, USA Institute for Integrative Genome Biology, University of California, Riverside, Riverside, California, USA joel.sachs@ucr.edu.
Joel L
JL
Sachs
D020369:Bradyrhizobium / Q000502:physiology*; D007887:Fabaceae / Q000382:microbiology* / Q000502:physiology; D009586:Nitrogen Fixation; D012231:Rhizobium / Q000502:physiology*; D058441:Rhizosphere; D053204:Root Nodules, Plant / Q000382:microbiology* / Q000502:physiology; D012988:Soil Microbiology; D013559:Symbiosis