The origins of uncooperative rhizobia

Abstract

Mutualisms are thought to be destabilized by exploitative mutants that receive benefits from partners without reciprocation. Nonetheless, there is surprisingly little evidence for the spread of exploitation in mutualist populations. In particular mutualisms, non‐beneficial partners are commonplace and this raises the question of whether exploitation is invading as an adaptive strategy. Here, we highlight the legume–rhizobium mutualism as a key test case. Rhizobial bacteria fix nitrogen in legume roots in exchange for carbon from their hosts. However, non‐beneficial rhizobia are widespread, including non‐fixing and non‐nodulating strains. Recent research has shown that legumes can punish some uncooperative rhizobia and substantially reduce their fitness, but these sanctions must not be universally effective. Important questions about uncooperative rhizobia remain unresolved. (1) Is it adaptive for rhizobia to be uncooperative with hosts? (2) Do uncooperative rhizobia evolve from cooperative ancestors? (3) What are the mechanisms of rhizobial exploitation? We describe experimental approaches and testable hypotheses that address these gaps in our knowledge.

Standing genetic variation in host preference for mutualist microbial symbionts

“…Despite the ubiquity of mutualisms in nature, partners are known to vary in the fitness rewards they provide [1,3], and phenotypes or species that exploit the mutualism are common (reviewed in [3]). Exploiters, by definition, are thought to have a fitness advantage over their mutualistic competitors because they receive benefits while providing fewer or no rewards to their interacting partners [3,4]. Because of the apparent fitness benefits of exploitation, mutualisms are predicted to be susceptible to invasion and spread of species or phenotypes that exploit the interaction [5][6][7][8][9][10], which could lead to a breakdown in the mutualism [11].…”

“…While there is debate on the origin and the maintenance of these mechanisms [20 -23], their viability as an evolutionary stable state [15][16][17]24], and how we can distinguish between them in natural systems [20,22,25], all three mechanisms share a common outcome: the host increases the relative fitness of more beneficial partners and/or decreases the relative fitness of less beneficial or exploitative partners. Given the recurrent observation of exploitative partners [4,8,26], selection on stabilizing mechanisms is predicted to be strong because exploitative symbionts are assumed to have negative effects on host fitness [13,16,[27][28][29][30] (but see [31]). If there is a cost to stabilizing mechanisms, in the absence of exploiters, selection will favour the loss of host stabilizing traits [17].…”

In Situ Phylogenetic Structure and Diversity of Wild Bradyrhizobium Communities

“…Rhizobia can achieve reproductive success via multiple lifestyles (12), including living free in the soil (14,44,53,62), on or near root surfaces (12,18,19,51), or in legume nodules (60). Least is known about rhizobia in bulk soil (not penetrated by plant roots).…”

“…While rhizobia can persist for years in soil without host legumes (12,30,61), it appears that growth is often negligible in bulk soil (4,10,14,22,25). Rhizobia can also proliferate in the rhizosphere (soil near the root zone) of legumes (4,10,18,19,22,25,51). Some rhizobia might specialize in rhizosphere growth and infect hosts only rarely (12,14,51), whereas other genotypes are clearly nonsymbiotic because they lack key genes (62) and must therefore persist in the soil.…”

“…Rhizobia can also proliferate in the rhizosphere (soil near the root zone) of legumes (4,10,18,19,22,25,51). Some rhizobia might specialize in rhizosphere growth and infect hosts only rarely (12,14,51), whereas other genotypes are clearly nonsymbiotic because they lack key genes (62) and must therefore persist in the soil. The best-understood rhizobial lifestyle is the root nodule symbiosis with legumes, which is thought to offer fitness rewards that are superior to life in the soil (12).…”