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.

No abstract

Bacteria live in complex multispecies communities. Intimately interacting bacterial cells are ubiquitous on biological and mineral surfaces in all habitats. Molecular and cellular biologists have unraveled some key mechanisms that modulate bacterial interactions, but the ecology and evolution of these associations remain poorly understood. One debate has focused on the relative importance of cooperation among cells in bacterial communities. Some researchers suggest that communication and cooperation, both within and among bacterial species, have produced emergent properties that give such groups a selective advantage. Evolutionary biologists have countered that the appearance of group-level traits should be viewed with caution, as natural selection almost invariably favors selfishness. A recent theory by Morris, Lenski, and Zinser, called the Black Queen Hypothesis, gives a new perspective on this debate (J. J. Morris, R. E. Lenski, and E. R. Zinser, mBio 3(2):e00036-12, 2012). These authors present a model that reshapes a decades-old idea: cooperation among species can be automatic and based upon purely selfish traits. Moreover, this hypothesis stands in contrast to the Red Queen Hypothesis, which states that species are in constant evolutionary conflict. Two assumptions serve as the core of the Black Queen model. First, bacterial functions are often leaky, such that cells unavoidably produce resources that benefit others. Second, the receivers of such by-products will tend to delete their own costly pathways for those products, thus building dependency into the interactions. Although not explicitly required in their model, an emergent prediction is that the initiation of such dependency can favor the spread of more obligate coevolved partnerships. This new paradigm suggests that bacteria might often form interdependent cooperative interactions in communities and moreover that bacterial cooperation should leave a clear genomic signature via complementary loss of shared diffusible functions.

Symbioses are modelled as evolutionarily and ecologically variable with fitness outcomes for hosts shifting on a continuum from mutualism to parasitism. In a classic example, rhizobia fix atmospheric nitrogen for legume hosts in exchange for photosynthetic carbon. Rhizobial infection often enhances legume growth, but hosts also incur interaction costs because of root tissues and or metabolites needed to support symbionts in planta. Rhizobia exhibit genetic variation in symbiotic effectiveness, and ecological changes in light or mineral nitrogen availability can also alter the benefits of rhizobial infection for hosts. The net effects of symbiosis thus can range from mutualistic to parasitic in a context-dependent manner. We tested the extent of the mutualism-parasitism continuum in the legume-rhizobium symbiosis and the degree to which host investment can shape its limits. We infected Lotus strigosus with sympatric Bradyrhizobium genotypes that vary in symbiotic effectiveness. Inoculations occurred under different mineral nitrogen and light regimes spanning ecologically relevant ranges. Net growth benefits of Bradyrhizobium infection varied for Lotus and were reduced or eliminated dependent on Bradyrhizobium genotype, mineral nitrogen and light availability. But we did not detect parasitism. Lotus proportionally reduced investment in Bradyrhizobium as net benefit from infection decreased. Lotus control occurred primarily after infection, via fine-scale modulation of nodule growth, as opposed to control over initial nodulation. Our results show how divestment of symbiosis by Lotus can prevent shifts to parasitism.

The patterns and drivers of bacterial strain dominance remain poorly understood in natural populations. Here, we cultured 1292 Bradyrhizobium isolates from symbiotic root nodules and the soil root interface of the host plant Acmispon strigosus across a >840-km transect in California. To investigate epidemiology and the potential role of accessory loci as epidemic drivers, isolates were genotyped at two chromosomal loci and were assayed for presence or absence of accessory Bsymbiosis island^loci that encode capacity to form nodules on hosts. We found that Bradyrhizobium populations were very diverse but dominated by few haplotypeswith a single Bepidemic^haplotype constituting nearly 30 % of collected isolates and spreading nearly statewide. In many Bradyrhizobium lineages, we inferred presence and absence of the symbiosis island suggesting recurrent evolutionary gain and or loss of symbiotic capacity. We did not find statistical phylogenetic evidence that the symbiosis island acquisition promotes strain dominance and both symbiotic and nonsymbiotic strains exhibited population dominance and spatial spread. Our dataset reveals that a strikingly few Bradyrhizobium genotypes can rapidly spread to dominate a landscape and suggests that these epidemics are not driven by the acquisition of accessory loci as occurs in key human pathogens.