Efficiency of partner choice and sanctions inLotusis not altered by nitrogen fertilization

Abstract

Eukaryotic hosts must exhibit control mechanisms to select against ineffective bacterial symbionts. Hosts can minimize infection by less-effective symbionts ( partner choice) and can divest of uncooperative bacteria after infection (sanctions). Yet, such host-control traits are predicted to be context dependent, especially if they are costly for hosts to express or maintain. Legumes form symbiosis with rhizobia that vary in symbiotic effectiveness (nitrogen fixation) and can enforce partner choice as well as sanctions. In nature, legumes acquire fixed nitrogen from both rhizobia and soils, and nitrogen deposition is rapidly enriching soils globally. If soil nitrogen is abundant, we predict host control to be downregulated, potentially allowing invasion of ineffective symbionts. We experimentally manipulated soil nitrogen to examine context dependence in host control. We co-inoculated Lotus strigosus from nitrogen depauperate soils with pairs of Bradyrhizobium strains that vary in symbiotic effectiveness and fertilized plants with either zero nitrogen or growth maximizing nitrogen. We found efficient partner choice and sanctions regardless of nitrogen fertilization, symbiotic partner combination or growth season. Strikingly, host control was efficient even when L. strigosus gained no significant benefit from rhizobial infection, suggesting that these traits are resilient to short-term changes in extrinsic nitrogen, whether natural or anthropogenic.

Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California

“…Several studies have uncovered rhizobial genotypes that achieve high frequency at localized sites [33,51,64], but haplotype G03_R01 dominates both locally and also across major ecological boundaries including mountain ranges and areas of inhospitable habitat. It is striking that haplotype G03_R01 was found in sites that vary markedly in their patterns of rainfall, temperature, plant community, and key soil nutrients [65,66], especially given that most of the Bradyrhizobium lineages that we uncovered were relatively localized in their distribution. Recent work that focused on non-symbiotic lineages of Bradyrhizobium in soils has also found evidence of widespread genotypes, suggesting that this might be a common pattern for these bacteria [37].…”

Standing genetic variation in host preference for mutualist microbial symbionts

“…Although evidence consistent with host stabilizing traits has been found in legumes [27][28][29][30]43], we have little empirical data to infer potential micro-evolutionary dynamics of these traits in natural host populations [19]. Our study has filled several important empirical gaps that are critical to understand any potential evolutionary dynamics of host stabilizing traits, by showing There is no evidence to suggest that selection will favour a loss in the ability to exclude exploitative partners in the absence of exploitation, as indicated by a lack evidence of fitness cost in the trait and the lack of potential correlated evolutionary responses with investment in total symbiotic associations.…”

“…Regus et al [43] suggests that partner choice is not plastic to environmental alterations in the costs and benefits of the mutualism. Consistent with partner choice and host sanctions, our data indicate that M. lupulina expresses significant genetic variation for the ability to filter out compatible exploitative partners and that selection will favour hosts with higher partner filtering, thus favouring a mutualism-stabilizing trait that reduces fitness rewards to exploiters.…”

“…Non-beneficial symbionts co-occur with beneficial partners in both natural and agricultural systems [36][37][38][39][40][41], and selection favours less beneficial rhizobia in the absence of mutualism-stabilizing mechanisms [42]. Empirical evidence also suggests that legumes possess stabilizing traits that reduce overall infection by less beneficial or non-beneficial partners, which is expected to stabilize the mutualism by reducing fitness rewards to non-beneficial genotypes and prevent them from spreading to fixation in populations [27][28][29][30]43]. Although the microevolution of stabilizing mechanisms will directly affect mutualism stability or breakdown, we have little data on whether they are genetically variable or subject to natural selection, and how they evolve in contemporary populations.…”

Nonnodulating Bradyrhizobium spp. Modulate the Benefits of Legume-Rhizobium Mutualism

“…Seed preparation and planting followed previously published methods (14). Inoculated plants received a total of 5 ϫ 10 8 rhizobial cells in 5 ml of ddH 2 O (equivalent by mass to ϳ10 6 cells g Ϫ1 soil), which is higher than most estimates of natural rhizobial soil populations (up to 10 5 nodulating cells g Ϫ1 soil) (31)(32)(33), but compensates for rhizobial attrition that occurs during the stressful inoculation process (10,14,20,30,(34)(35)(36).…”