Origins of cheating and loss of symbiosis in wild Bradyrhizobium

• Published in: Journal of evolutionary biology 2010-05, Vol.23 (5), p.1075-1089
• Main Authors: SACHS, J.L, EHINGER, M.O, SIMMS, E.L
• Format: Article
• Language: English
• Subjects: Adaptation, Biological - genetics; Adaptation, Biological - physiology; Agriculture; Bacteria; Base Sequence; Bayes Theorem; Bradyrhizobium; Bradyrhizobium - genetics; Bradyrhizobium - physiology; California; CheA protein; cheating; DNA Primers - genetics; Evolution; Evolutionary biology; exploitation of mutualism; Fitness; Gene transfer; Gene Transfer, Horizontal - genetics; horizontal gene transmission; Legumes; Likelihood Functions; Loteae - microbiology; Lotus strigosus; Models, Genetic; Molecular Sequence Data; Mutants; mutualism breakdown; Nitrogen; Nodulation; Nutrients; parasitism; Photosynthates; Phylogeny; Population biology; rhizobia; Root Nodules, Plant - microbiology; Root Nodules, Plant - physiology; Roots; Sequence Analysis, DNA; Soil; Symbionts; Symbiosis; symbiosis island
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/j.1420-9101.2010.01980.x

Rhizobial bacteria nodulate legume roots and fix nitrogen in exchange for photosynthates. These symbionts are infectiously acquired from the environment and in such cases selection models predict evolutionary spread of uncooperative mutants. Uncooperative rhizobia - including nonfixing and non-nodulating strains - appear common in agriculture, yet their population biology and origins remain unknown in natural soils. Here, a phylogenetically broad sample of 62 wild-collected rhizobial isolates was experimentally inoculated onto Lotus strigosus to assess their nodulation ability and effects on host growth. A cheater strain was discovered that proliferated in host tissue while offering no benefit; its fitness was superior to that of beneficial strains. Phylogenetic reconstruction of Bradyrhizobium rDNA and transmissible symbiosis-island loci suggest that the cheater evolved via symbiotic gene transfer. Many strains were also identified that failed to nodulate L. strigosus, and it appears that nodulation ability on this host has been recurrently lost in the symbiont population. This is the first study to reveal the adaptive nature of rhizobial cheating and to trace the evolutionary origins of uncooperative rhizobial mutants.