Cooperation in the Rhizosphere and the “Free Rider” Problem

Abstract

Rhizobial bacteria, endomycorrhizal fungi (also known as arbuscular mycorrhizas), and pseudomonad bacteria associated with plant roots can provide substantial benefits to the plants by fixing nitrogen, supplying phosphorus, or controlling root pathogens, respectively. A significant fraction of plant photosynthetic carbon may be used by these associated microorganisms, both to support their beneficial activities and for microbial growth and reproduction. Because many microbial individuals are associated with each individual plant, the individual benefit to a microbe that allocates more resources to its own reproduction (thereby allocating less to fixing N2, supplying P, or producing antifungal metabolites) would exceed its individual loss from any resulting reduction in collective benefits (mainly plant carbon substrates). An initially rare “free rider” mutant strain might therefore be expected to displace its more cooperative parental strain. Yet, the mycorrhizal and legume–rhizobium mutualisms have persisted (often coexisting with “cheating”) for millions of years. This paper discusses the importance of microbial cooperation (with plants and with other microbes) and possible reasons for its evolutionary persistence in the rhizosphere. In undisturbed soils, spatial structure can favor kin selection, but this may be counterbalanced by the increased likelihood that future competitors will be among the beneficiaries of current cooperation. In loose associations, direct fitness benefits to microorganisms may explain the evolutionary persistence of activities (e.g., production of antifungal compounds) that can benefit plants as a side effect. In closer, more symbiotic, relationships, host sanctions against individuals or clones that fail to perform their symbiotic function may be more important. New molecular methods and other research tools are facilitating research on this topic, and some of these conclusions soon may be revised. Corresponding Editor: D. A. Phillips. For reprints of this Special Feature, see footnote 1, p. 815

Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms

“…Respiration in support of Ni fixation for the benefit of the plant is expensive for rhizobia (Gutschick 1981), consuming C compounds that they could otherwise have used to support their own reproduction (Denison 2000, Kretovich et al 1977). If some strains can limit costs by "free-riding" on other strains, they will be favored by selection and spread (Denison et al 2003a). However, cheating is far from universal.…”

“…Such multiple infections can create a potential tragedy of the commons (Hardin 1968). The tragedy is that cooperative partners that supply their hosts with resources indirectly aid competing strains (including noncooperative ones) colonizing the same individual (Denison et al 2003a). Within-host competition can therefore destabilize mutualisms (West et al 2002a,b).…”

“…This is why models based on a single clone of symbiont per host are irrelevant to most rhizosphere mutualisms, which involve multiple strains per plant. The evolutionary consequences of hosting multiple partners is a recurring theme in rhizosphere mutualisms (Denison 2000, Denison et al 2003a, Kiers et al 2002, Sachs et al 2004). This review discusses the tragedy of the commons in plant-rhizosphere mutualisms and its various solutions.…”

Carbon Fluxes in the Rhizosphere

“…Given the known wide range of association types between roots and rhizosphere biota from highly mutualistic (e.g., rhizobium-legume) to totally opportunistic (e.g., free-living bacteria), we know little about how these different types of associations operate in determining the amount and the types of rhizosphere C flows, not to mention the potential role of the complex interactions in the rhizosphere through evolutionary time. This complexity and the associated opportunities for future research are well illustrated in the case of "the free rider" problem in the recent paper by Denison et al (2003). The "free rider" problem arises when considering microbial intra-species competition in the context of plant-microbe cooperation and mutualisms.…”

“…Yet, this reasoning directly contradicts the fact that plant-microbe cooperation and mutualisms have persisted, presumably, for millions of years. Using this apparent paradox as a thread, Denison et al (2003) discussed potential mechanisms of plant-microbe cooperation and mutualisms and touched on many intricate connections in the rhizosphere.…”