Ecological drivers of the evolution of symbiosis

Beneficial symbioses are widespread in nature and underpin the function of both natural and manmade ecosystems. Moreover, by providing the interacting species with new ecological functions, symbiosis represents an important source of innovation and has thus played a crucial role in the evolution of life on Earth.

Although beneficial symbioses are important, their evolution is hard to explain because it requires for once independent species to overcome their self-interest and become an integrated organism. A simple but so far untested idea for how stable beneficial symbioses might evolve is that they start off as exploitative interactions, wherein the host organism captures and exploits their symbiont for the beneficial function they provide. If the environment inside the host is sufficiently different to that experienced outside the host, the symbiont will over time adapt to this new niche and in so doing lose their ability to thrive outside the host due to trade-offs between the different traits required to survive in each environment. Through this process, the fitness interests of the host and symbiont species become aligned such that each now relies upon the other. Testing this idea in most symbiotic interactions is impossible because they originated millions of years ago and now the species cannot be separated to test for adaptation to free-living environments.

In this project we overcome this challenge by using an experimentally tractable microbial symbiosis between the single-celled ciliate host Paramecium and the green alga Chlorella, which can either live inside the host cell (intracellular niche) or live freely in freshwater (extracellular niche). We will sample free-living and symbiotic algal populations from UK lakes, and compare their adaptation to key environmental parameters predicted to vary between the intracellular and extracellular niches. Using comparative genomics we will identify the patterns of genome divergence between the symbiotic and free-living algae and identify genetic adaptations to the symbiotic and free-living lifestyles. Finally, we will experimentally evolve symbiotic algae in the laboratory under free-living environmental conditions to test if this leads to the loss of their symbiotic ability through trade-offs.

Together these experiments will advance our understanding of the biology of symbioses, helping to solve the long-standing evolutionary puzzle of how and why symbioses originate and evolve. In so doing the research will also provide insight into how symbioses and the important functions they perform can be maintained in natural and man-made ecosystems.

Symbiosis plays an important role in the function of a wide range of natural ecosystems. Moreover, symbiosis is an important mechanism of evolutionary innovation and directly led to major evolutionary transitions in organismal complexity (e.g. evolution of the eukaryotic cell). Despite the major importance of symbiosis in the history of life on earth and its contemporary relevance to a wide range of applied problems (e.g. maintaining agricultural productivity legume-rhizhobial and plant-mycorrhizal symbioses) it is poorly understood by the general public. Furthermore, protist-algal symbioses represent a relatively untapped resource of biodiversity for biotechnological exploitation. We have identified 3 groups of non-academic beneficiaries:

Biotechnology: Microalgae are of interest to bio-based industry because of their ability to sustainably produce an array of natural products using just sunlight, CO2 and a few nutrients. We will actively engage with commercialisation activities through the Algal Biotechnology Sheffield network (ABS - https://www.sheffield.ac.uk/algae) and AlgaeUK (https://www.algae-uk.org.uk; a BBSRC NIBB) which are focused on translating academic knowledge in high value products from microalgae into industrial applications. We will engage with a wide range of microalgae-focused bio-based industrial partners from within the Algae-UK network. To lead this activity, we have included an Impact Co-Investigator, Dr. Pandhal, from the Department of Chemical and Biological Engineering, who is a lead researcher in ABS and sits on the Algae-UK Management Board.

Secondary school children: Teaching of evolution in Key Stages 2 and 3 of the National Curriculum is mainly theoretical and lacking in engaging practical classes. We will take evolution experiments into the school classroom allowing pupils to measure the fitness effects of symbiosis themselves, generating excitement about microbes and evolution and offering deeper experiential learning.

General public: Protecting and conserving biodiversity and the valuable functions that it performs requires more than simply conserving individual taxa, rather it is vital to conserve ecosystems and the species interactions they contain. This is particularly true for symbiosis. Conserving symbiotic species interactions is essential for conserving coral reefs and rainforests, as well as for keeping food on our tables through agricultural symbioses of plants with microbes. Our public engagement strategy will raise awareness of the role of symbiosis in the function of natural ecosystems.