Evolutionary and ecological feedbacks across tripartite interactions in the rhizobial community
Lead Research Organisation:
University of Sheffield
Department Name: School of Biosciences
Abstract
Many organisms engage in symbioses; intimate partnerships with another species that can be mutually beneficial to both partners. However, these relationships do not occur in isolation, but are embedded within a network of interacting species, which can shape the evolution of symbiotic partnerships. The relationship between nitrogen-fixing bacteria (rhizobia) and legumes (e.g. peas and beans) is arguably one of the most economically important examples of symbiosis. Rhizobia take nitrogen from the air and convert it into a form that plants can use. This is exchanged with the plant in return for nutrients and shelter in specialized organs called root nodules. By providing the plant with a supply of nitrogen these bacteria effectively act as 'biofertilisers', reducing the need for expensive and environmentally damaging applications of chemical fertiliser to legumes as well as the non-legume crops grown alongside them.
Rhizobia do not only interact with their plant hosts however. When not living in the plant's root nodules, rhizobia live freely in the soil, interacting with the diverse microbial community that exists there. Key members of all soil microbe communities are the temperate phages, viruses that infect bacteria. These viruses can have widespread and various effects on their bacterial hosts. On the one hand they can be antagonistic, killing their host in order to produce more viral particles that will go on to infect new cells. Surprisingly however these viruses can also be beneficial. Every so often, upon infecting a bacterial cell, rather than reproducing to make more viral particles, they will integrate their own DNA into the bacterial genome, giving the bacteria access to novel genes and effectively becoming viral weapons that bacteria can use against their competitors. Rhizobia therefore engage in two important and highly contrasting interactions, with their legume hosts and with temperate phages. These separate interactions will place different selection pressures on the bacterial population and consequently are likely to have important implications for one another. This project will unpick this temperate phage - rhizobia - legume relationship in order to understand how this tripartite community shapes, and is shaped by, its constituent interactions.
This project will combine studies using highly controlled lab experiments with studies of natural and semi-natural communities. Lab experiments allow hypotheses to be directly tested and, due to the high turnover of generations in bacteria, bacteria-phage coevolution to be observed in real time. Meanwhile, experiments conducted in the 'wild' or by bringing natural communities into the lab demonstrate how real communities are structured and behave. In combination these approaches offer a powerful way of exploring these complex interactions.
This work will provide the first comprehensive examination of the role of temperate phages in rhizobial populations. With the rise in global food demand, understanding what shapes the ecology and evolution of symbiotic microbes such as rhizobia will be increasingly important. This work will therefore lay the foundation for exploring what roles the wider microbial community plays in these processes. This will lead to future work examining how we can apply these lessons to sustainable agricultural practices. For example, by using temperate phages to enhance the effectiveness of biofertilisers.
Rhizobia do not only interact with their plant hosts however. When not living in the plant's root nodules, rhizobia live freely in the soil, interacting with the diverse microbial community that exists there. Key members of all soil microbe communities are the temperate phages, viruses that infect bacteria. These viruses can have widespread and various effects on their bacterial hosts. On the one hand they can be antagonistic, killing their host in order to produce more viral particles that will go on to infect new cells. Surprisingly however these viruses can also be beneficial. Every so often, upon infecting a bacterial cell, rather than reproducing to make more viral particles, they will integrate their own DNA into the bacterial genome, giving the bacteria access to novel genes and effectively becoming viral weapons that bacteria can use against their competitors. Rhizobia therefore engage in two important and highly contrasting interactions, with their legume hosts and with temperate phages. These separate interactions will place different selection pressures on the bacterial population and consequently are likely to have important implications for one another. This project will unpick this temperate phage - rhizobia - legume relationship in order to understand how this tripartite community shapes, and is shaped by, its constituent interactions.
This project will combine studies using highly controlled lab experiments with studies of natural and semi-natural communities. Lab experiments allow hypotheses to be directly tested and, due to the high turnover of generations in bacteria, bacteria-phage coevolution to be observed in real time. Meanwhile, experiments conducted in the 'wild' or by bringing natural communities into the lab demonstrate how real communities are structured and behave. In combination these approaches offer a powerful way of exploring these complex interactions.
This work will provide the first comprehensive examination of the role of temperate phages in rhizobial populations. With the rise in global food demand, understanding what shapes the ecology and evolution of symbiotic microbes such as rhizobia will be increasingly important. This work will therefore lay the foundation for exploring what roles the wider microbial community plays in these processes. This will lead to future work examining how we can apply these lessons to sustainable agricultural practices. For example, by using temperate phages to enhance the effectiveness of biofertilisers.
Planned Impact
Impact on the general public:
I have a strong track record of engaging in outreach activities both within schools and with the public and intend to build on this to communicate future work. I will collaborate with the Widening Participation (WP) team at the university to develop and implement lesson plans for school-aged students. The WP team run well established, award winning initiatives aimed at inspiring children from backgrounds under-represented in academia, including those from low income areas and ethnic minorities, to engage with STEM subjects. Programs such as Green Apples and Realising Opportunities work with schools from around the country to offer pupils the opportunity to visit the university and learn about the research being conducted. I also have established links with colleges in underprivileged areas of London (Bsix, Hackney and the Robert Clack School, Dagenham) where I organise and run events for A-level students on evolutionary themes to encourage participation in STEM subjects at degree level. I will develop activity sessions on the theme of symbiosis, using games and conversation to challenge pupils to think critically about why species choose to interact and why sometimes this breaks down.
York hosts numerous forums for public engagement that are run annually, including the York Festival of Ideas and Pint of Science, which this year I ran a successful publicity campaign for. These events provide a framework in which outreach activities can be developed and delivered to a wide audience, as they have an established reputation for excellent and innovative science out reach. I will develop an interactive event to explore the diversity and importance of symbiotic interactions, from cooperation to conflict, in nature.
Impact on the agricultural community:
Though the aims of this project are predominantly 'blue skies' it will lay the ground work for future work addressing the role of within-soil interactions on the rhizobia-legume symbiosis. York-based organizations, including the N8 AgriFood Resiliance Programme, White Rose Consortium, FERA and YESI provide an interface between academia and industry. In particular schemes such as the N8 employ dedicated Knowledge Exchange teams who aim to facilitate collaboration between researchers, stakeholders and industry. I have also established links with companies, such as Legume Technology Ltd a UK based bio-inoculant company.
Through these links I will pursue partners for collaborations to translate the proof-of-concept findings from this project into field and applied studies addressing how temperate phages can impact agricultural production and sustainability. Potential projects include:
- Investigating the impact of agricultural management strategies (i.e. population mixing through tillage vs no-till farming) and phages on rhizobial population structure.
- The application of temperate phages to increase competitiveness of rhizobial seed innocula, by increasing bacterial competiveness in the soil (through increased phage resistance and acting as antimicrobial agents) and increase symbiotic function in the host (through HGT of symbiosis functions).
To establish these collaborative projects I will seek funding from sources such as the N8 pump priming scheme and BES small grant scheme as well as upcoming special interest calls, for instance through Innovate UK funding schemes. In addition the N8 program also offers opportunities to engage with the end users of research through both workshops and engagement events.
I have a strong track record of engaging in outreach activities both within schools and with the public and intend to build on this to communicate future work. I will collaborate with the Widening Participation (WP) team at the university to develop and implement lesson plans for school-aged students. The WP team run well established, award winning initiatives aimed at inspiring children from backgrounds under-represented in academia, including those from low income areas and ethnic minorities, to engage with STEM subjects. Programs such as Green Apples and Realising Opportunities work with schools from around the country to offer pupils the opportunity to visit the university and learn about the research being conducted. I also have established links with colleges in underprivileged areas of London (Bsix, Hackney and the Robert Clack School, Dagenham) where I organise and run events for A-level students on evolutionary themes to encourage participation in STEM subjects at degree level. I will develop activity sessions on the theme of symbiosis, using games and conversation to challenge pupils to think critically about why species choose to interact and why sometimes this breaks down.
York hosts numerous forums for public engagement that are run annually, including the York Festival of Ideas and Pint of Science, which this year I ran a successful publicity campaign for. These events provide a framework in which outreach activities can be developed and delivered to a wide audience, as they have an established reputation for excellent and innovative science out reach. I will develop an interactive event to explore the diversity and importance of symbiotic interactions, from cooperation to conflict, in nature.
Impact on the agricultural community:
Though the aims of this project are predominantly 'blue skies' it will lay the ground work for future work addressing the role of within-soil interactions on the rhizobia-legume symbiosis. York-based organizations, including the N8 AgriFood Resiliance Programme, White Rose Consortium, FERA and YESI provide an interface between academia and industry. In particular schemes such as the N8 employ dedicated Knowledge Exchange teams who aim to facilitate collaboration between researchers, stakeholders and industry. I have also established links with companies, such as Legume Technology Ltd a UK based bio-inoculant company.
Through these links I will pursue partners for collaborations to translate the proof-of-concept findings from this project into field and applied studies addressing how temperate phages can impact agricultural production and sustainability. Potential projects include:
- Investigating the impact of agricultural management strategies (i.e. population mixing through tillage vs no-till farming) and phages on rhizobial population structure.
- The application of temperate phages to increase competitiveness of rhizobial seed innocula, by increasing bacterial competiveness in the soil (through increased phage resistance and acting as antimicrobial agents) and increase symbiotic function in the host (through HGT of symbiosis functions).
To establish these collaborative projects I will seek funding from sources such as the N8 pump priming scheme and BES small grant scheme as well as upcoming special interest calls, for instance through Innovate UK funding schemes. In addition the N8 program also offers opportunities to engage with the end users of research through both workshops and engagement events.
People |
ORCID iD |
Ellie Harrison (Principal Investigator / Fellow) |
Publications
Billane K
(2022)
Why do plasmids manipulate the expression of bacterial phenotypes?
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Brockhurst MA
(2019)
The Ecology and Evolution of Pangenomes.
in Current biology : CB
Brockhurst MA
(2022)
Ecological and evolutionary solutions to the plasmid paradox.
in Trends in microbiology
Fields B
(2021)
The impact of intra-specific diversity in the rhizobia-legume symbiosis.
in Microbiology (Reading, England)
Fields B
(2022)
Genetic variation is associated with differences in facilitative and competitive interactions in the Rhizobium leguminosarum species complex.
in Environmental microbiology
Ford S
(2021)
Introducing a Novel, Broad Host Range Temperate Phage Family Infecting Rhizobium leguminosarum and Beyond.
in Frontiers in microbiology
Hall JPJ
(2022)
Introduction: the secret lives of microbial mobile genetic elements.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Harrison E
(2017)
Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger.
in BioEssays : news and reviews in molecular, cellular and developmental biology
Harrison E
(2018)
Migration promotes plasmid stability under spatially heterogeneous positive selection.
in Proceedings. Biological sciences
Stevenson C
(2018)
Plasmid stability is enhanced by higher-frequency pulses of positive selection.
in Proceedings. Biological sciences
Description | ACCE2 NERC DTP studentship - The impact of antagonistic bacteria-phage coevolution on the rhizobia-legume symbiosis |
Amount | £89,960 (GBP) |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 09/2021 |
End | 02/2025 |
Description | Institute for Sustainable Food PhD funding |
Amount | £153,803 (GBP) |
Organisation | University of Sheffield |
Department | Institute for Sustainable Food |
Sector | Academic/University |
Country | United Kingdom |
Start | 10/2019 |
End | 06/2023 |
Description | NERC ACCE2 DTP |
Amount | £89,844 (GBP) |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 10/2019 |
End | 10/2023 |
Description | Plasmid manipulation of bacterial gene regulatory networks |
Amount | £248,963 (GBP) |
Funding ID | BB/R014884/2 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 06/2020 |
End | 12/2022 |
Description | The role of evolutionary refinement in horizontal gene transfer of rhizobial symbiosis genes |
Amount | £90,435 (GBP) |
Funding ID | NE/X009971/1 |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 05/2023 |
End | 05/2024 |
Description | BBSRC seed funding - diversification of arable rotations |
Organisation | University of Sheffield |
Department | Sheffield Biorepository |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Design and implementation of experiments to test the impact of arable leys on the growth of native and foriegn legume crops and KE event |
Collaborator Contribution | Design and implementation of experiments to test the impact of arable leys on the growth of native and foriegn legume crops and KE event |
Impact | KE event (see communication). |
Start Year | 2022 |
Description | Bradyrhizobium DTP |
Organisation | James Hutton Institute |
Country | United Kingdom |
Sector | Charity/Non Profit |
PI Contribution | I established a partnership with researchers at the JHI Dundee and an inoculum company to put togeather an application for a studentship. I put forward the ideas, designed the experimental plan and will be the primary supervisor of the student. |
Collaborator Contribution | My partners at JHI will provide strains that we will work with, samples from prior work and expert advice. In the latter part of the project they will host and train the student in field techniques and provide access to field sites. The partners in PlantWorksUK will provide inocula for us to test, supplement the research budget by £1000pa and host the student for a 3 month industrial placement. |
Impact | The student has been hired and is due to start in october 2019 |
Start Year | 2019 |
Description | Bradyrhizobium DTP |
Organisation | Plantworks Ltd UK |
Country | United Kingdom |
Sector | Private |
PI Contribution | I established a partnership with researchers at the JHI Dundee and an inoculum company to put togeather an application for a studentship. I put forward the ideas, designed the experimental plan and will be the primary supervisor of the student. |
Collaborator Contribution | My partners at JHI will provide strains that we will work with, samples from prior work and expert advice. In the latter part of the project they will host and train the student in field techniques and provide access to field sites. The partners in PlantWorksUK will provide inocula for us to test, supplement the research budget by £1000pa and host the student for a 3 month industrial placement. |
Impact | The student has been hired and is due to start in october 2019 |
Start Year | 2019 |
Description | Evolutionary refinement in symbiosis |
Organisation | University of Calgary |
Country | Canada |
Sector | Academic/University |
PI Contribution | I am leading the project and was awarded funding |
Collaborator Contribution | My collaborators are supplying strains and expertise to facilitate the project |
Impact | NA |
Start Year | 2023 |
Description | How do interactions with phages in the soil impact the rhizobia-legume symbiosis |
Organisation | University of York |
Department | Department of Biology |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Primary supervision of shared student |
Collaborator Contribution | Cosupervision of PhD student. Responsible for developing experiments with phage communities |
Impact | no outputs yet |
Start Year | 2021 |
Description | Diversifying arable rotation knowledge exchange meeting |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Industry/Business |
Results and Impact | 2 day knowledge exchange workshop run as part of a collaboration awarded BBSRC seed funding. The workshop was aimed at farmers and those working in the agricultural sector to discuss the potential roles of legumes in UK rotations. I co-organised, facilitated and spoke at the event. Discussions lead to identification of key research priorities for follow-up projects and lead to greater understanding on my side about the practical challenges to growing more legumes in the UK. |
Year(s) Of Engagement Activity | 2023 |
Description | Participation in production of science comic |
Form Of Engagement Activity | Engagement focused website, blog or social media channel |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Schools |
Results and Impact | Working with a comic artists who specialise in science outreach we produced a comic that depicts the adventures of two siblings discovering the world of microbes and how they evolve. It is accompanied by a website, currently being finalised. This will provide further resources that can be used by schools to build lessons around the area of microbial diversity and evolution. THe comic and website will be launched in the coming months. |
Year(s) Of Engagement Activity | 2021 |
Description | Postcast interview, Society for General Microbiology |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Media (as a channel to the public) |
Results and Impact | Interview with the Society for General Microbiology podcast. Talking about the importance of soil microbes for plants and agriculture and strategies for improving, maintaining or hacking the soil microbiome to increase health and function. |
Year(s) Of Engagement Activity | 2020 |
Description | Rhizobia-Legume interactions stand at the Discovery Night, Sheffield. |
Form Of Engagement Activity | Participation in an open day or visit at my research institution |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Public/other audiences |
Results and Impact | This is part of a science activity evening that engages families and children (5 - 10 year olds) with hands on science. The event is run by the university and features talks, interactive activities and demonstrations. Students in my lab prepared a stand explaining the importance of rhizobia, and soil microbes generally, for plant growth. This includes plants grown in transparent media so that people can see rhizobia in action, root nodules to handle and squash, as well as posters and games about the symbiosis. |
Year(s) Of Engagement Activity | 2020 |
URL | https://www.sheffield.ac.uk/discoverynight |