Ecological drivers of intragenomic conflict resolution

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences

Abstract

The classical view of evolution is as a process of gradual accumulation of small changes by mutations passed on to descendants. However, genome sequencing has revealed that in bacteria genes are frequently exchanged between cells and species by a process called horizontal gene transfer, allowing evolution to make big, fast jumps. Genes often pass from one bacterial cell to another on circular pieces of DNA called plasmids. However, acquiring a plasmid can be costly to a bacterial cell because plasmids use energy and introduce new genes that disrupt the normal working of the bacterium. In evolutionary theory these costs are called intragenomic conflicts because what is good for the plasmid is bad for the bacterial chromosome, and vice versa. We have recently shown that evolution can resolve these conflicts by a process of 'compensatory evolution', whereby either the bacterial chromosome or the plasmid gains mutations that lessen the cost of carrying the plasmid. By increasing plasmid survival, compensatory evolution is likely to increase the chance of new genes jumping onto plasmids from bacterial chromosomes, allowing these to be shared with other species in the community. In this proposal we will discover how the ecology of microbial communities and the environments they live in shape the processes of compensatory evolution, and whether compensatory evolution itself speeds up the sharing of genes between species.

Planned Impact

Who will benefit from this research and how?

This is basic blue-skies research that will advance fundamental understanding of evolutionary processes and dynamics in bacterial communities. Nevertheless, bacterial evolution has a broad range of important impacts upon society, for example through the effects of rapid evolutionary change on the prognosis of clinical infections, the evolutionary emergence of antibiotic resistance, and evolutionary responses of microbial communities underpinning the functioning of ecosystems to environmental change. Despite the widespread and fundamental impact of rapid microbial evolution in general and horizontal gene transfer (HGT) in particular upon society, these evolutionary processes remain very poorly understood by the general public and policy-makers. The key benefits deriving from this research will therefore be increased knowledge and understanding of bacterial evolution among the following groups:

Secondary school age 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 experimental evolution into the school classroom allowing pupils to experience evolution in action themselves in real time, generating excitement about microbes and evolution and offering deeper experiential learning.

General public: Bacterial evolution is high on the news agenda due to the crisis in antimicrobial resistance (AMR), however few non-scientists realise that this societal problem is exacerbated by HGT-mediated evolution. Public engagement activities will enhance public understanding of HGT and put this into the context of AMR to show what we can all do to reduce the risks of AMR.

Policy makers in healthcare and agri-food sectors: HGT impacts the evolutionary emergence of AMR in the clinic and the spread of functional traits in soil bacterial communities. Designing policies and interventions that aim to e.g. limit the spread of AMR or conserve the functional diversity of soil bacterial communities, requires sharing knowledge and understanding of the dynamics of HGT and how these are shaped by the ecology of microbial communities and their environments arising from this research with stakeholders and policymakers in these sectors. We will engage with healthcare stakeholders via an established clinical network (PARC; PI Brockhurst is a member) and agri-food stakeholders via the N8 AgriFood Partnership facilitated by the N8 AgriFood Knowledge Exchange Fellows.

Related Projects

Project Reference Relationship Related To Start End Award Value
NE/R008825/1 01/02/2018 31/05/2020 £487,227
NE/R008825/2 Transfer NE/R008825/1 01/06/2020 31/10/2021 £149,022
 
Description Bacteria rapidly adapt to new environments increasing their fitness. We show that this process of environmental adaptation is prevented by the presence of other bacterial species in simple communities in soil microcosms. Published in Evolution Letters.
Acquisition of plasmids causes costs for the host cell which can be ameliorated by mutations elsewhere in the genome (compensatory mutations). Using mathematical models we show that plasmid survival is enhanced when these compensatory mutations are encoded on the plasmid itself, rather than on the bacterial chromosome. Published in mSystems.
Bacteria rapidly adapt to the costs of acquiring plasmids to overcome intragenomic conflict. Published in Microbiology.
We also published a major review on the ecology and evolution of pangenomes focusing on the importance of intragenomic conflicts and horizontal gene transfer. Published in Current Biology.
Exploitation Route These findings advance understanding of how species evolve in complex communities, which is relevant to understanding how species will adapt to anthropogenic environmental change. These findings advance understanding of how plasmids survive and spread in bacterial populations/communities, which is relevant to understanding the spread of antibiotic resistance genes.
Sectors Environment,Healthcare

 
Description The findings from this project have been delivered to the public through outreach activities and helped increase understanding of the role for microbes in health (of soils, plants and animals). The findings have fed into a Parliamentary Office of Science and Technology POSTnote.
First Year Of Impact 2019
Sector Agriculture, Food and Drink,Environment
Impact Types Societal,Policy & public services

 
Description Interactive microbiome exhibit (Great Yorkshire Show) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact 630 people visited our interactive exhibit about the important role that microbiomes play in health (in general encompassing soils, plants and animals) as part of the Discovery Zone. This was aimed at secondary school children but attended by a wider range of ages including adults. The exhibit sparked questions and discussion.
Year(s) Of Engagement Activity 2019
 
Description Sustaining the soil microbiome POSTnote 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Policymakers/politicians
Results and Impact Parliamentary Office of Science and Technology Note (POSTnote) entitled "Susutaining the soil microbiome" authored by Cagla Stevenson (PhD student) in my group
Year(s) Of Engagement Activity 2019
URL https://researchbriefings.parliament.uk/ResearchBriefing/Summary/POST-PN-0601