Microbial evolution and transitions along the parasite-mutualist continuum

Abstract

Virtually all plants and animals, including humans, are home to symbiotic microorganisms. Symbiotic interactions can be neutral, harmful or have beneficial effects on the host organism. However, growing evidence suggests that microbial symbionts can evolve rapidly, resulting in drastic transitions along the parasite-mutualist continuum. In this Review, we integrate theoretical and empirical findings to discuss the mechanisms underpinning these evolutionary shifts, as well as the ecological drivers and why some host-microorganism interactions may be stuck at the end of the continuum. In addition to having biomedical consequences, understanding the dynamic life of microorganisms reveals how symbioses can shape an organism's biology and the entire community, particularly in a changing world.

Fig. 1. Evolutionary transitions onto and along the parasite–mutualist continuum.

Examples from nature of microorganisms transitioning from free-living to host-associated lifestyles include the evolution of parasitic species in the Bacillus cereus group (for example, the causative agent of anthrax) from soil-dwelling ancestors (part a), and environmental Pantoea bacteria evolving obligate mutualistic roles in stink bug growth and development (part b). Examples involving transitions along the continuum are the widespread plant parasite Pseudomonas syringae likely evolving from mutualistic ancestors, driven by horizontal gene transfer (HGT) of type III secretion systems^, (part c), and entomopathogens taking over the metabolic role of an ancient and degraded endosymbiont in cicadas (part d). Image credits: part a (right) Getty images Smith Collection/Gado.Contributor; part b is adapted from ref., CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/); part c (left), image courtesey of Gerald Holmes; part c (right) is adapted from ref., CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/); part d (left), image courtesey of Yu Matsuura; part d (right) adapted with permission from ref., PNAS.

Fig. 2. Transitions in a community context.

Defensive symbioses involve multiple species, including a host (H) and defensive microorganism (DM) that protects against an attacking parasite (P). Often, hidden players exist within a DM, such as mobile genetic elements (MGEs; for example phages, plasmids and transposable elements) that encode factors involved in the protective function of the DM. In this community, the evolutionary and ecological moves (examples denoted by arrows) of each player can affect the relative position of another on the parasite–mutualist continuum. Players may move, resulting in an overall beneficial (net+), detrimental (net–) or negligible (net 0) effect on host fitness. For example, if a MGE encodes key protective functions, then its loss (move 2) will shift the DM’s position towards parasitism (all cost and no benefit to host). Meanwhile, the costs of P to H will increase now that H is no longer protected by the DM and its MGE. Transitions here can also alter the coevolutionary patterns and processes between players and species.