Intra- and inter-specific competition and the evolution of cooperation in Bacillus thuringiensis
Lead Research Organisation:
Royal Holloway University of London
Department Name: Biological Sciences
Abstract
Cooperation is a common feature of bacterial lifestyles. This may be particularly true of bacteria that cause diseases (pathogenic bacteria) and of beneficial bacteria that live in close association with larger hosts (symbiotic bacteria). Many of the essential tools that enable bacteria to exploit hosts are based on what can be called 'public goods'. These are enzymes or toxins and other compounds that bacteria must export outside the cell in order to break open host cells and harvest the resources. Bacteria also export chemical signals that communicate information about their abundance within hosts to other bacteria and may thereby coordinate attack. Efficient use of hosts therefore requires bacteria to act collectively, if a low proportion of bacteria fail to cooperate bacterial infections should to be less successful and produce fewer infections in new hosts. These public goods are expensive to make in terms of resources. In evolutionary terms cooperation can be unstable because bacteria may leave more offspring within hosts if they 'cheat' and fail to contribute to these expensive cooperative products. Evolutionary theory has made predictions about how cooperation could be maintained. If most infections are established by close relatives with similar strategies, metabolically expensive cooperation will benefit their relative and they, in turn will then spread the genes for cooperation. In addition, while competition within hosts can lead to selection for cheating, competition between groups of bacteria inhabiting different hosts will select for groups that exploit their host more efficiently, and which therefore cooperate. The evolutionary forces that can maintain cooperation between hosts and symbiotic bacteria are diverse. However, one possible mechanism is that host can discriminate between bacteria that are exploitative or not and produce increased immune responses against symbionts that are not cooperative. I propose to test these evolutionary ideas on cooperation, in relation to the production of toxins, antibiotics and chemical signals. Prelimary data also indicate that the exploitation of hosts by Bt is strongly affect by competition with symbionts such as P. agglomerans. I will test how competition with symbionts affects the expression of cooperative toxins. Conversely, these symbionts can cooperate with Bt rather than continue to cooperate with hosts as gut symbionts. I will test how host insects react to infections with 'cheating' symbionts. I will use a study system which is familiar to me and also of environmental and medical importance. This system is the insect-killing bacteria Baccillus thuringiensis, a caterpillar host (the larvae of the diamondback moth) and the gut symbiont Pantoea agglomerans. B. thuringiensis (Bt) is used as a biological pesticide. It is applied against pests in horticulture, forestry and fruit productionan and against mosquito larvae. It has an excellent safety record, it does not harm humans, animals or beneficial insect predators and is licensed as an organic spray. While Bt pesticides are efficient at killing pests they are relatively poor at being transmitted as a disease from pest to pest after spraying. Improved transmission would have many benefits for the ability of Bt to control pests. Preliminary data in my laboratory suggests that cooperative traits are vital for efficient transmission between hosts, as the above theory predicts. An understanding of how cooperation maintains efficient transmission and transmission maintains cooperation could therefore be vital to understanding how to improve its use. Bt is closely related to the bacteria that causes anthrax, Bacillus anthracis and to Bacillus cereus, several strains of which cause food-poisoning in humans. These human pathogens use very similar biochemical machinery to Bt and a understanding of how these bacteria cooperate to exploit hosts may eventually be of medical significance.
People |
ORCID iD |
Benjamin Raymond (Principal Investigator) |
Publications
Deng C
(2015)
Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain.
in The ISME journal
Garbutt J
(2011)
Antagonistic competition moderates virulence in Bacillus thuringiensis.
in Ecology letters
MARTINOU A
(2010)
Impact of intraguild predation on parasitoid foraging behaviour
in Ecological Entomology
Medaney F
(2016)
Ecological and genetic determinants of plasmid distribution in Escherichia coli.
in Environmental microbiology
Medaney F
(2016)
Live to cheat another day: bacterial dormancy facilitates the social exploitation of ß-lactamases.
in The ISME journal
Mikonranta L
(2019)
Targeting antibiotic resistant bacteria with phage reduces bacterial density in an insect host.
in Biology letters
Méric G
(2018)
Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group.
in Molecular ecology
Raymond B
(2010)
Bacillus thuringiensis: an impotent pathogen?
in Trends in microbiology
Raymond B
(2008)
Moderation of pathogen-induced mortality: the role of density in Bacillus thuringiensis virulence
in Biology Letters
Raymond B
(2012)
The dynamics of cooperative bacterial virulence in the field.
in Science (New York, N.Y.)
Raymond B
(2013)
Cooperation and the evolutionary ecology of bacterial virulence: the Bacillus cereus group as a novel study system.
in BioEssays : news and reviews in molecular, cellular and developmental biology
Raymond B
(2010)
Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field.
in PLoS pathogens
Raymond B
(2009)
A mid-gut microbiota is not required for the pathogenicity of Bacillus thuringiensis to diamondback moth larvae.
in Environmental microbiology
Raymond B
(2009)
Environmental Impact of Genetically Modified Crops
Raymond B
(2017)
In defense of Bacillus thuringiensis, the safest and most successful microbial insecticide available to humanity - a response to EFSA.
in FEMS microbiology ecology
Raymond B
(2018)
An appeal for a more evidence based approach to biopesticide safety in the EU.
in FEMS microbiology ecology
Raymond B
(2011)
Effects of host plant and genetic background on the fitness costs of resistance to Bacillus thuringiensis.
in Heredity
Raymond B.
(2009)
Resistance management of transgenic insect-Resistant crops: Ecological factors
in Environmental Impact of Genetically Modified Crops
Shapiro-Ilan D
(2016)
Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes.
in Evolutionary applications
Van Leeuwen E
(2015)
Making pathogens sociable: the [corrected] emergence of high relatedness through limited host invasibility.
in The ISME journal
Zhou L
(2014)
The social biology of quorum sensing in a naturalistic host pathogen system.
in Current biology : CB
Zhou L
(2018)
Combining the high-dose/refuge strategy and self-limiting transgenic insects in resistance management-A test in experimental mesocosms.
in Evolutionary applications
Description | We have found out that models of social conflicts, cheating cooperation etc, can be particularly informative for understanding the virulence of parasites, as investment in microbial virulence can often be seen as a joint cooperative venture. This key understanding has diverse implications for how we might be able to manipulate virulence, particularly for biological control agents, as well as how strategies to suppress microbial virulence might affect the long-term evolutionary trajectory of parasites. |
Exploitation Route | Currently we are exploring ways of taking these findings forward in terms of improving biological control agents. This has led to a funded Leverhulme grant award in which we are applying the principles of social evolution / group selection to select for improved killing power in microbial control agents. We have been applying these methods to develop bacterial strains that can overcome resistance in a target pest. This has proved to be highly successfull with gains in killing power of new mutants in excess of 100x. Currently we are exploring options for protecting some of the intellectual property associated with these methods. |
Sectors | Agriculture Food and Drink Environment Healthcare Pharmaceuticals and Medical Biotechnology |
Description | This research has revealed a great deal about the maintenance of virulence in bacteria and biological control agents. While this has not had an immediate impact yet, this award has informed future proposals on biological pesticide improvement (see Leverhume RPG-1014-252) and may yet have an impact on virulence management. Further collaborations have now established that a social evolution may be important for understanding the stability of virulence in entomopathogenic nematodes. We anticipate that these results may have relevance and impact in how researchers and industry bodies attempt to culture and improve their biocontrol agents. We have now submitted a patent application (founded on the principles established in this fellowship) and have attracted funding for a PhD studentship to apply social evolution theory to the improvement of fungal entomopathogens. |
First Year Of Impact | 2014 |
Sector | Agriculture, Food and Drink,Creative Economy |
Impact Types | Economic |
Description | Advising stakeholders & EU commission on biosafety of microbial pesticides |
Geographic Reach | Europe |
Policy Influence Type | Contribution to a national consultation/review |
Impact | Certain EU members states have been agitating for tightening up the regulations on the application of microbial bicontrol agents in particular Bacillus thuringiensis (Bt). This position was in part driven by misconstruing the basis of some food poisoning incidents in Germany. I presented evidence to industry and to a meeting involving regulators, scientists and stakeholders. My evidence and analysis confirms the excellent safety record of Bt and unpicked the very poor evidence linking Bt to food poisoing or other disease. Following this consultation the EU have not taken the decision to tighten up regulations, a decision that faciltates the use of environmentally friendly biological alternatives to chemical insecticides. My responses to the European Food Safety Authority on the biological safety of Bt have been published in FEMS Microbiology and Ecology. |
Description | Membership of ACRE- DEFRA committee on release of GMOs and biological control agents |
Geographic Reach | National |
Policy Influence Type | Participation in a guidance/advisory committee |
Description | AHDB studentship scheme |
Amount | £71,400 (GBP) |
Organisation | Agricultural and Horticulture Development Board |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 09/2018 |
End | 09/2021 |
Description | Group selection as a novel tool to screen and improve biological pesticides |
Amount | £371,386 (GBP) |
Funding ID | BB/S002928/1 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 12/2018 |
End | 11/2022 |
Description | Leverhulme Standard grant |
Amount | £233,233 (GBP) |
Funding ID | RPG-2014-252 |
Organisation | The Leverhulme Trust |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 01/2015 |
End | 12/2018 |
Title | Stable red/green marker plasmids |
Description | We have engineered stable marker plasmids for Bacillus thuringiensis / B. cereus that express RFP or GFP as well as distinct antibiotic resistance plasmids. These are particularly useful for carrying out competition experiments or exploring the ecology and function of these bacteria in containment. |
Type Of Material | Technology assay or reagent |
Year Produced | 2016 |
Provided To Others? | Yes |
Impact | see Zhou et al 2014 Curr Biol |
Description | Industrial Partnership - (as part of BBSRC IPA award) |
Organisation | Dow AgroSiences |
Country | United Kingdom |
Sector | Private |
PI Contribution | My team will be engaged in producing mutants with increased virulence to resistant insect pests, as well as screening strain collections and toxin libraries for novel or improved isolates and proteins. |
Collaborator Contribution | The partner will be providing access to a sequenced strain collection as welll as to additional sequencing / molecular characaterization services. |
Impact | not yet....project began end of Feb 2019 |
Start Year | 2019 |
Description | Social biology of virulence in entomopathogenic nematodes |
Organisation | U.S. Department of Agriculture USDA |
Department | Agricultural Research Service |
Country | United States |
Sector | Public |
PI Contribution | I developed and designed experiments that would investigate the problem of unstable virulence in entomopathogenic nematodes. I have then analysed the data coming out of these experiments |
Collaborator Contribution | My partner (David Shapiro-Ilan) and his laboratory carried out the selection experiments. |
Impact | We have identified a major possible cause of the loss of virulence in these important biocontrol agents. We expect this to have real implications for how industry and researchers maintain effective populations of nematodes. This work has now resulted in a publication Shapiro-Ilan & Raymond (2016) |
Start Year | 2012 |
Description | The evolutionary ecology of quorum sensing in vivo |
Organisation | French National Institute of Agricultural Research |
Department | INRA Versailles |
Country | France |
Sector | Academic/University |
PI Contribution | We have brought ecological and evolutionary perspectives to the understanding of the function of quorum-sensing during in vivo infections. Our contribution has included many experiments exploring the fitness of diverse mutants and examining the distribution and structure of early stage Bacillus infections. |
Collaborator Contribution | Our partners contributed important genetic tools (an array of mutants), technical expertise and training for one of my PhD students. |
Impact | Thus far the collaboration has resulted in one high impact publication (Zhou et al 2014, Curr Biol) and we have another manuscript in preparation. We also have a joint grant proposal in review. The colloboration is multidisciplinary and involves molecular biologists, geneticists and evolutionary ecologists. |
Start Year | 2011 |
Description | Wuhan plasmid project |
Organisation | Huazhong Agricultural University |
Department | State Key Laboratory of Agricultural Microbiology |
Country | China |
Sector | Academic/University |
PI Contribution | Shaped research questions, wrote paper, shaped and informed analysis |
Collaborator Contribution | Collected genomic data, analysed data, co-wrote paper |
Impact | This has resulted in a publication in mBio (Zheng et al)- and is a collaboration between molecular biologists and myself as an evolutionary ecologists. Other projects related to this collaboration are still ongoing. |
Start Year | 2016 |
Title | BIOPESTICIDES |
Description | The present invention relates to Bacillus thuringiensis strains which are phenotypically stable and have increased virulence compared to the wild-type strains, whereby the increased virulence has been achieved by the exposure of the strain to a mutagen during one or more passages. Such strains are particularly useful as biopesticides. Methods for increasing virulence in microbial pesticides are also described. |
IP Reference | WO2019030529 |
Protection | Patent application published |
Year Protection Granted | 2019 |
Licensed | No |
Impact | This application has helped us in negotiations with commercial companies including Dow Agroscience and Bayer. |
Description | IBMA Copa-Cogeca workshop |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Industry/Business |
Results and Impact | Safety and regulation of Bt based biopesticides were discussed with stakeholders and presented to representatives of EU commission |
Year(s) Of Engagement Activity | 2017 |
URL | http://www.ibma-global.org/en/news/ibma-and-copa-cogeca-workshop-to-explore-the-implications-of-baci... |
Description | IBMA industry conference |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Industry/Business |
Results and Impact | This is the international biocontrol manufacturers annual meeting and very much an industry meeting rather than an academic conference. I was invited to give a talk on the safety on micro-organisms in biocontrol |
Year(s) Of Engagement Activity | 2017 |
URL | http://www.abim.ch |
Description | Open days |
Form Of Engagement Activity | Participation in an open day or visit at my research institution |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Undergraduate students |
Results and Impact | The Penryn campus runs a series of open days throughtout the year designed to engage with prospective students and their families. This gives us a venue in which to talk about our research generally and that of the campus. In an event last summer, for instance, I discussed the recent invasion of diamond back moth and met with a local cabbage farmer and talked about pest control issues associated with this species. |
Year(s) Of Engagement Activity | 2016,2017,2018 |
Description | Presentation of results to biological control community |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | I gave a plenary talk at an international organization of biological control meeting, which is attended by practitioners, biocontrol companies as well as academics. This led to the collaboration with a USDA lab on entomopathogenic nematode virulence. |
Year(s) Of Engagement Activity | 2010 |
Description | Pursuing industrial collaborators for biopesticide development |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | Yes |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | This has led to the submission of a BBRSR industrial partnership award project with Syngenta, which unfortunately was not funded. More recent applications have attracted expressions of interest or informal support from Dow Agroscience. As yet impacts are unknown, but we have developed a wider network of contacts in industry that might help us commercialize any future research findings. |
Year(s) Of Engagement Activity | 2009,2011,2012,2013,2014 |
Description | Silwood Bugs Day |
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 | Industry/Business |
Results and Impact | 100-200 members of the public attended a Silwood Park open day focussed on entomological research at Imperial. As well as academic staff local research organizations, charities and conservation organizations had stands. The local MP and councillors also attended. |
Year(s) Of Engagement Activity | 2015 |
Description | Visit and planning meeting with biopesticide producers |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Industry/Business |
Results and Impact | Attended meeting at eNema HQ in Kiel, Germany. eNema are one of the largest producers of biopesticides in the EU. We discussed my recent results with nematodes and Bacillus and agreed to collaborate on a BBSRC proposal investigating nematode improvement for corn rootworm pests. |
Year(s) Of Engagement Activity | 2015 |
Description | Workshop meeting with CABI |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Third sector organisations |
Results and Impact | 5-6 members of staff from Silwood Park attended a workshop run by CABI, a leading international biological control organization based in Egham. The purpose of the meeting was to explore future avenues for collaboration between academia and the needs of this sector. |
Year(s) Of Engagement Activity | 2015 |
Description | invited research application - Bayer |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Industry/Business |
Results and Impact | My research group was invited to pitch for research funding from Bayer in order to pursue research avenues following on from work on evoltuion of virulence in microbial insecticides. This involved preliminary meetings, a Skype presentation to the company and the submission of a research proposal. This proposal is still under consideration, and was submitted late last year. |
Year(s) Of Engagement Activity | 2018 |