Recurrent mutualism breakdown events in a legume rhizobia metapopulation

Abstract

Bacterial mutualists generate major fitness benefits for eukaryotes, reshaping the host phenotype and its interactions with the environment. Yet, microbial mutualist populations are predicted to generate mutants that defect from providing costly services to hosts while maintaining the capacity to exploit host resources. Here, we examined the mutualist service of symbiotic nitrogen fixation in a metapopulation of root-nodulating <i>Bradyrhizobium</i> spp<i>.</i> that associate with the native legume <i>Acmispon strigosus</i>. We quantified mutualism traits of 85 <i>Bradyrhizobium</i> isolates gathered from a 700 km transect in California spanning 10 sampled <i>A. strigosus</i> populations. We clonally inoculated each <i>Bradyrhizobium</i> isolate onto <i>A. strigosus</i> hosts and quantified nodulation capacity and net effects of infection, including host growth and isotopic nitrogen concentration. Six <i>Bradyrhizobium</i> isolates from five populations were categorized as ineffective because they formed nodules but did not enhance host growth via nitrogen fixation. Six additional isolates from three populations failed to form root nodules. Phylogenetic reconstruction inferred two types of mutualism breakdown, including three to four independent losses of effectiveness and five losses of nodulation capacity on <i>A. strigosus</i>. The evolutionary and genomic drivers of these mutualism breakdown events remain poorly understood.