Origins of cheating and loss of symbiosis in wildBradyrhizobium

Abstract

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.

Novel Burkholderia bacteria isolated from Lebeckia ambigua – A perennial suffrutescent legume of the fynbos

“…Thirdly, they may have entered the nodule as co-inoculants with other nodulating strains (Bai et al, 2003;Denton et al, 2003;Dudeja et al, 2012;Egamberdieva et al, 2010;Sturz et al, 1997). Finally they may be rhizobial strains which have lost the capacity to nodulate upon sub-culture (Howieson et al, 2000b;Sachs et al, 2010). Two non-nodulating strains (WSM4181 and WSM4182) arose from the same nodule as the effective strain WSM4186 (data not shown) which suggests that co-occupation could be a possibility.…”

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

“…A subset of isolates (75) were previously assessed using greenhouse nodulation assays on A. strigosus, which has already been shown to be a permissive host on diverse Bradyrhizobium [24,43,44]. Here, we conducted greenhouse nodulation experiments on an additional 55 isolates, using identical procedures.…”

“…The remaining 342 root surface isolates were classified as symbiotic or non-symbiotic based on success or failure of PCR amplification of at least one symbiosis island locus (nifD, nodD-A, nodZ, and nolL) [22,24,45]. Earlier analyses showed that successful amplification of these loci, giving a band of the correct size, is a reliable indicator of presence of the symbiosis island [24]. Many isolates were tested at two or more loci (160/342; Table S1).…”

“…Symbiosis loci required for host nodulation and nitrogen fixation are clustered onto large plasmids or genomic islands [15][16][17][18][19], that can be transferred among lineages, presumably via conjugation [20][21][22]. Non-nodulating rhizobia are also common [23,24], and these strains often lack some or all of the characterized symbiosis loci [23][24][25][26][27][28].…”

Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils

“…Nevertheless, the hypothesized ecological roles of these populations remain focused on symbiosis. Similarly, previous studies have isolated Bradyrhizobium strains diminished or lacking in the ability to fix nitrogen or nodulate leguminous plants from soil, but these strains were described consistently as having transiently abandoned a symbiotic lifestyle or as relics of an ancestral symbiotic genotype (Sachs et al, 2010(Sachs et al, , 2011Okubo et al, 2012).…”