The symbiont side of symbiosis: do microbes really benefit?

Abstract

Microbial associations are integral to all eukaryotes. Mutualism, the interaction of two species for the benefit of both, is an important aspect of microbial associations, with evidence that multicellular organisms in particular benefit from microbes. However, the microbe's perspective has largely been ignored, and it is unknown whether most microbial symbionts benefit from their associations with hosts. It has been presumed that microbial symbionts receive host-derived nutrients or a competition-free environment with reduced predation, but there have been few empirical tests, or even critical assessments, of these assumptions. We evaluate these hypotheses based on available evidence, which indicate reduced competition and predation are not universal benefits for symbionts. Some symbionts do receive nutrients from their host, but this has not always been linked to a corresponding increase in symbiont fitness. We recommend experiments to test symbiont fitness using current experimental systems of symbiosis and detail considerations for other systems. Incorporating symbiont fitness into symbiosis research will provide insight into the evolution of mutualistic interactions and cooperation in general.

Keywords: endosymbiosis; host–microbe interactions; microbial fitness; mutualism; symbiont transmission.

FIGURE 1

(A) Experimental designs to test the effect of symbiosis on host fitness (left) and symbiont fitness (right). Both experiments involve measuring growth or other fitness parameters (see section Recommendations for Investigating Symbiont Fitness) in the presence and absence of their partner. Experiments on host fitness have been performed in diverse systems, but the equivalent symbiont fitness experiment is rarely performed. (B) Experimental design from Wollenberg and Ruby (2012) for measuring the relative growth of two groups of bobtail squid symbionts within naturally infected hosts. Competition assays were performed to test within-host fitness by inoculating the seawater of a hatchling squid with a symbiont strain from each symbiont group (left). A separate experiment confirmed that the symbionts had an equal ability to colonize the squid after single-strain inoculations (not pictured). Symbiont growth was tested in the environment by inoculating filtered (middle) and unfiltered (right) seawater from the natural habitat of the squid and symbiont.