Host-symbiont coevolution: Exploring the parasitism-mutualism continuum

Lead Research Organisation: University of Liverpool
Department Name: Sch of Biological Sciences

Abstract

Intimate and prolonged associations between different organisms - symbioses - are widespread and important in the natural environment. Symbiotic associations can range from being parasitic, where one organism benefits at the expense of the other, to being mutualistic, where both organisms benefit from the association. Such symbiotic associations underpin the functioning of ecosystems: mutualism can allow pairs of organisms to survive where otherwise neither would and parasitism can limit the growth of host populations. These symbioses are particularly important in microbial communities but little is known about how these associations shape the evolution and diversity of microbial symbionts. Here we want to understand how the evolution of symbiotic organisms is different under conditions that range from parasitic to mutualistic. Our approach is to study the evolution of a bacterial-plasmid symbiosis where the nature of the association ranges from parasitic to mutualistic depending on the environment: in the presence of mercury the association is mutualistic because the plasmid has a gene for mercury resistance; and in the absence of mercury the association is parasitic because carrying the plasmid slows the growth of the bacteria. In nature carrying the plasmid allows bacteria to survive in otherwise toxic mercury contaminated soils. We will exploit the short generation times, and large population sizes of bacteria to observe evolution in action. We will discover and contrast the genetic changes that occur in the genomes of both the bacteria and the plasmid as they co-evolve on a continuum of environments that change the symbiosis from parasitic to mutualistic. - Our study is novel because we will, for the first time, study evolution across a parasitic-mutualistic symbiosis continuum using a single symbiotic association. - Our study is relevant to the natural environment because such bacterial-plasmid associations are widespread, but poorly understood, in microbial communities and are likely to play an important role in maintaining biodiversity and ecosystem function, particularly in response to heavy metal contamination of soils. - Our study is powerful because we will use an experimental approach to study evolution in action. - Our study is timely because we will exploit the latest technologies in DNA sequencing to directly observe evolution of genetic sequences in bacterial and plasmid genomes.

Publications

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Related Projects

Project Reference Relationship Related To Start End Award Value
NE/H005080/1 05/07/2010 31/07/2012 £367,469
NE/H005080/2 Transfer NE/H005080/1 01/08/2012 31/05/2014 £118,081
 
Description Our main finding is that bacteria adapt to carrying plasmids by gaining chromosomal mutations that switch off expression of genes on the chromosome. These mutations reduce the cost of carrying the plasmid and mean that plasmids can persist even in environments where they were originally very costly. This evolutionary solution occurs rapidly and in parallel across a wide range of environments including conditions where the plasmid is parasitic or mutualistic. Published in Current Biology (2015). We have used individual based simulation modelling to further demonstrate the conditions for compensatory evolution to occur. Published in Mobile Genetic Elements (2016).

We have developed mathematical models and computer simulations of plasmid ecology, tested by experiments, which show that bacteriophages limit the conditions under which plasmids can persist. Concomitantly plasmids impair the ability of bacteria to evolve resistance to bacteriophages. Published in mBio and Biology Letters (both papers 2015). Using genome sequencing of these evolved populations we have shown that together phages and plasmids impede the bacterial evolutionary responses seen in pairwise interactions suggesting that evolution in complex microbial communities will be hard to predict due to conflicting selection pressures. Published in Molecular Ecology (2017)

We have shown extensive genetic sequence and phenotypic diversity among a community of coexisting environmental mercury resistance plasmids with implications for understanding the diversity of mobile genetic elements in nature. Published in Environmental Microbiology (2015).

We have shown that fluctuating environments affect the dynamics of host-parasite coevolution by impeding the spread of beneficial mutations in host populations. This work has been published in Proceedings of the Royal Society B (Harrison et al. 2013).

We have published several reviews of the literature concerning the topics of bacteria-plasmid coevolution (published in Trends in Microbiology), experimental coevolution of species interactions (published in Trends in Ecology and Evolution) and the adaptation of viruses to their hosts (Current Opinion in Virology).
Exploitation Route The ecology of plasmids is important for understanding bacterial evolution particularly because antibiotic resistance is often carried on plasmids. Our findings suggest that costs of plasmids can be rapidly compensated, potentially explaining why antibiotic resistance plasmids may persist long after the relevant (e.g. drug) selection is relieved, but also suggest the bacteriophages could be used to purge antibiotic resistance plasmids. Both of these possibilities should be tested in future work.
Sectors Environment,Healthcare

 
Description The findings of this research fed into public engagement activities including (1) a collaboration with artist Laurence Payot, LIVING SCULPTURES, about symbiosis which involved over 200 participants making sculptures and was displayed to public audiences at York Festival of Ideas 2014, Sheffield Festival of the Mind 2014, and The Bluecoat Gallery Liverpool; total audience approx. 5000, funded by grants from Arts Council England and The Wellcome Trust and providing 60 days of employment for artists; (2) a collaboration with artist Becs Andrews Company, TRANSMISSION, a dance performance, film and interactive audiovisual installation about disease transmission which has been shown at York Festival of Ideas 2014 and Manchester Science Festival 2014 and is available online (http://www.artplayer.tv/video/956/becs-andrews-company-transmission), total audience to date is approx. 7000, funded by grants from Arts Council England and The Wellcome Trust and resulting in 300 days of employment for artists and performers.
First Year Of Impact 2014
Sector Creative Economy,Education,Leisure Activities, including Sports, Recreation and Tourism,Culture, Heritage, Museums and Collections
Impact Types Cultural

 
Description Consolidator Grant
Amount € 1,230,000 (EUR)
Funding ID Agreement N°311490-COEVOCON 
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 02/2013 
End 01/2018
 
Description School visits, Evolution under the Microscope, London UK 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact More than 100 pupils from two London schools (BSix College Hackney, Robert Clack School Dagenham) attended a series of 3 interactive sessions about Evolution Under the Microscope, featuring research from this award
Year(s) Of Engagement Activity 2015