Mucin-derived sialic acid metabolism in gut bacteria
Lead Research Organisation:
Quadram Institute
Department Name: Gut Microbes and Health
Abstract
The gastrointestinal (GI) tract is colonized by a diverse community of microbes (called the gut microbiota) whose composition has a profound impact on human health. The composition of the human gut microbiota is greatly influenced by the degradation of complex dietary and host carbohydrates in the gut. Bacteria associated with the lining of the gut have the ability to forage on sugar chains provided by the mucus layer covering the GI tract.
Sialic acid or N-acetylneuraminic acid (Neu5Ac) is an abundant sugar residue found in terminal location of mucin carbohydrate chains and a key target of intestinal bacteria. Sialic acid catabolism by bacterial sialidases releases free Neu5Ac from mucins which availability in the mucosal environment drives intestinal inflammation and infection. For example, elevated levels of free sialic acid in the gut, during and post antibiotic treatments, promote the expansion of Clostridium difficile and Salmonella, as these bacteria lack a sialidase (but possess the machinery allowing the bacteria to utilise free Neu5Ac) and thus rely on free Neu5Ac released from mucins by members of the gut microbiota.
We recently discovered an unusual sialidase activity in gut commensal bacteria, which instead of releasing free Neu5Ac as in the case of hydrolytic sialidases, produces a transglycosylation product, 2,7-anhydro-Neu5Ac from mucins, which classifies this enzyme as an intramolecular trans-sialidase (IT-sialidase).
The aim of the proposal is to characterise at the molecular level how 2,7-anhydro-Neu5Ac is utilised by gut bacteria and test the hypothesis that IT-sialidase will i) provide gut bacteria with a major nutritional advantage in vivo by enabling them to produce and utilise 2,7-anhydro-Neu5Ac from mucins in a selfish manner and ii) limit enteric pathogens outgrowth by reducing the availability of Neu5Ac (and starving them as a result).
Specifically, this project aims to answer the following questions:
1. What is the pathway for 2,7-anhydro-Neu5Ac metabolism in R. gnavus?
2. Which gut bacteria are able to utilise 2,7-anhydro-Neu5Ac as sole source of nutrient?
3. Do IT-sialidases confer gut bacteria with a competitive advantage in vivo?
4. What is the impact of R. gnavus strains on the level of free sialic acid in the gut?
5. Can IT-sialidase producing strains impair S. Typhimurium colonisation in vivo?
The project is divided into 3 objectives to address these questions.
In the first objective, we will exploit our recombinant IT-sialidase to enzymatically synthesise 2,7-anhydro-Neu5Ac (not commercially available) in suitable amount to biochemically study the metabolic pathways in our model organism R. gnavus, identify and characterise the proteins involved in this process.
We will then expand this work to the gut microbiota by using a combination of bioinformatics analyses coupled with stable isotope probing (SIP) and experimental validation in vitro to identify which other commensal bacteria from the human gut are able to utilise 2,7-anhydro-Neu5Ac.
Building from our in vitro data (published and preliminary), we will then perform experiments in mouse models to determine the impact of the IT-sialidase-expressing microbes on their ability to colonise the mucosal layer, modulate the level of sialic acid in the gut, and reduce Salmonella infection.
This basic knowledge is important to explore novel anti-infective approaches as alternatives to antibiotics, which alleviate the risk of antimicrobial resistance (AMR) by modulating the mucosal environment rather than targeting the pathogen per se.
Sialic acid or N-acetylneuraminic acid (Neu5Ac) is an abundant sugar residue found in terminal location of mucin carbohydrate chains and a key target of intestinal bacteria. Sialic acid catabolism by bacterial sialidases releases free Neu5Ac from mucins which availability in the mucosal environment drives intestinal inflammation and infection. For example, elevated levels of free sialic acid in the gut, during and post antibiotic treatments, promote the expansion of Clostridium difficile and Salmonella, as these bacteria lack a sialidase (but possess the machinery allowing the bacteria to utilise free Neu5Ac) and thus rely on free Neu5Ac released from mucins by members of the gut microbiota.
We recently discovered an unusual sialidase activity in gut commensal bacteria, which instead of releasing free Neu5Ac as in the case of hydrolytic sialidases, produces a transglycosylation product, 2,7-anhydro-Neu5Ac from mucins, which classifies this enzyme as an intramolecular trans-sialidase (IT-sialidase).
The aim of the proposal is to characterise at the molecular level how 2,7-anhydro-Neu5Ac is utilised by gut bacteria and test the hypothesis that IT-sialidase will i) provide gut bacteria with a major nutritional advantage in vivo by enabling them to produce and utilise 2,7-anhydro-Neu5Ac from mucins in a selfish manner and ii) limit enteric pathogens outgrowth by reducing the availability of Neu5Ac (and starving them as a result).
Specifically, this project aims to answer the following questions:
1. What is the pathway for 2,7-anhydro-Neu5Ac metabolism in R. gnavus?
2. Which gut bacteria are able to utilise 2,7-anhydro-Neu5Ac as sole source of nutrient?
3. Do IT-sialidases confer gut bacteria with a competitive advantage in vivo?
4. What is the impact of R. gnavus strains on the level of free sialic acid in the gut?
5. Can IT-sialidase producing strains impair S. Typhimurium colonisation in vivo?
The project is divided into 3 objectives to address these questions.
In the first objective, we will exploit our recombinant IT-sialidase to enzymatically synthesise 2,7-anhydro-Neu5Ac (not commercially available) in suitable amount to biochemically study the metabolic pathways in our model organism R. gnavus, identify and characterise the proteins involved in this process.
We will then expand this work to the gut microbiota by using a combination of bioinformatics analyses coupled with stable isotope probing (SIP) and experimental validation in vitro to identify which other commensal bacteria from the human gut are able to utilise 2,7-anhydro-Neu5Ac.
Building from our in vitro data (published and preliminary), we will then perform experiments in mouse models to determine the impact of the IT-sialidase-expressing microbes on their ability to colonise the mucosal layer, modulate the level of sialic acid in the gut, and reduce Salmonella infection.
This basic knowledge is important to explore novel anti-infective approaches as alternatives to antibiotics, which alleviate the risk of antimicrobial resistance (AMR) by modulating the mucosal environment rather than targeting the pathogen per se.
Technical Summary
The mammalian intestinal tract is protected by a mucus layer, which contains heavily glycosylated mucin proteins that comprise up to 80% carbohydrate and are often terminated by sialic acid residues. The most abundant sialic acid is N-acetylneuraminic acid (Neu5Ac) which can serve as an energy source by commensal and pathogenic bacteria. The availability of sialic acid in the mucosal compartment is particular important for the proliferation of enteropathogenic bacteria during infection. We recently discovered an usual sialidase activity in Ruminococcus gnavus, which instead of releasing free sialic acid, produces a trans-glycosylation product, 2,7-anhydro-Neu5Ac specifically from alpha-2-3-linked sialylated substrates, which classifies this enzyme as an intramolecular trans-sialidase and recently confirmed that 2,7-anhydro-Neu5Ac was used as a substrate by R. gnavus. Our bioinformatics analysis showed that IT-sialidases are predicted to occur in 11% of bacterial metagenomes examined, suggesting that bacterial IT-sialidases may play a key role in driving symbiotic host associations. This project will (1) examine the mechanisms and occurrence of IT-sialidase mediated sialic acid metabolism in gut bacteria, (2) test the hypothesis that it provides a competitive nutritional advantage to the bacteria and (3) investigate how this directly affects the level of sialic acid in the gut and impact on pathogens in vivo. Outcomes of the project will provide an enhanced understanding of sialic acid metabolism in the intestinal ecosystem and a molecular route to devise alternative strategies to antibiotics for reducing or preventing enteric infection and antimicrobial resistance.
Planned Impact
Public Health
Infectious diseases are a growing public health issue due to increasing global anti-microbial resistance (AMR). In humans, microbial infection typically starts with bacteria interacting with the mucosal surfaces which are more exposed and prone to infection. Elevated levels of sialic acid are induced by antibiotic therapy and pathogen infection. Therefore, reducing the amount of sialic acid in the mucosal environment is a novel strategy to reduce microbial infection. Currently much effort is centred upon developing new anti-microbial agents. This work will provide a completely novel approach to alleviate the risk of AMR by modulating the mucosal environment rather than targeting the pathogen per se. Within the timeframe of this study, we will focus on Salmonella for which antimicrobial resistance to cephalosporin has greatly increased. Other antibiotic-associated enteric pathogens include Clostridium difficile, an ubiquitous organism that recently emerged in animals and in humans as the main cause of nosocomial diarrhoea. In the last decade incidences of C. difficile infections (CDI) increased markedly, partly due to the use of antimicrobials, in particular cephalosporins. Future applications could target multi-drug resistant pathogens targeting other mucosal sites in the body such as Staphylococcus aureus, an ubiquitous bacterial pathogen that also uses sialic acid as nutrient source, and respiratory pathogens including Hemophilus influenzae, Streptococcus pneumoniae, or Pseudomonas aeruginosa which induce expression of sialic acid as adhesion sites. The longer-term application of this research will be designing and testing suitable routes and pharmaceutical formulations for IT-sialidase mucosal delivery depending on the site of the infection. These could include the use of pre/probiotic/synbiotic approaches in the gut or aerosol in the airways.
Carbohydrate/Enzyme biotech companies
The outcomes of this work will be of direct interest to companies commercializing novel glycoenzymes (e.g. trans-sialidases) (e.g. Prozomix, Megazyme, Nzytech) and those developing effective bioassays, glycosidase inhibitors, and carbohydrate-based diagnostics and therapeutics (e.g. Ludger; Iceni Diagnosis), or speciality carbohydrates such as sialylated oligosaccharides (e.g. Glycom, Carbosynth, Inbiose) for potential application as neutraceutical, pharmaceutical and cosmetic ingredients.
Biopharmaceutical/drug companies
The research may also be of interest to biopharmaceutical companies (e.g. GlaxoSmithKline) developing novel sialidase (or neuraminidase) inhibitors incl. Influenza neuraminidase inhibitors.
Food and Healthcare companies (Probiotics/Microbiome)
This research may also be of interest to companies interested in modulating the gut microbiome via pro/prebiotic approaches (e.g. Danone, Nestle, Yakult) but also an increasing number of biotech startups operating in the emerging gut microbiome space (e.g. MicroBiome Therapeutics, Enterome Bioscience).
Early career researcher
This project will provide a unique training opportunity for a post-doctoral scientist to work in a multidisciplinary environment spanning research Labs at IFR and UEA (BIO and ENV). There will also be opportunities for undergraduate students (from UEA) and visiting scientists to gain research experience through short-term placements. The PDRA will receive expert training in anaerobic microbiology, heterologous expression, carbohydrate biosynthesis and analysis (HPLC, MS- and NMR-based methods), enzymatic assays, bioinformatics (TGAC) and statistical analyses. The techniques are well-established and there is considerable expertise in conducting research on glycobiology and gut microbiology. There will be opportunities to collaborate with chemists and structural biologists. The PDRA will benefit from the established international network of academic and industrial collaborations of the NRP Labs.
Infectious diseases are a growing public health issue due to increasing global anti-microbial resistance (AMR). In humans, microbial infection typically starts with bacteria interacting with the mucosal surfaces which are more exposed and prone to infection. Elevated levels of sialic acid are induced by antibiotic therapy and pathogen infection. Therefore, reducing the amount of sialic acid in the mucosal environment is a novel strategy to reduce microbial infection. Currently much effort is centred upon developing new anti-microbial agents. This work will provide a completely novel approach to alleviate the risk of AMR by modulating the mucosal environment rather than targeting the pathogen per se. Within the timeframe of this study, we will focus on Salmonella for which antimicrobial resistance to cephalosporin has greatly increased. Other antibiotic-associated enteric pathogens include Clostridium difficile, an ubiquitous organism that recently emerged in animals and in humans as the main cause of nosocomial diarrhoea. In the last decade incidences of C. difficile infections (CDI) increased markedly, partly due to the use of antimicrobials, in particular cephalosporins. Future applications could target multi-drug resistant pathogens targeting other mucosal sites in the body such as Staphylococcus aureus, an ubiquitous bacterial pathogen that also uses sialic acid as nutrient source, and respiratory pathogens including Hemophilus influenzae, Streptococcus pneumoniae, or Pseudomonas aeruginosa which induce expression of sialic acid as adhesion sites. The longer-term application of this research will be designing and testing suitable routes and pharmaceutical formulations for IT-sialidase mucosal delivery depending on the site of the infection. These could include the use of pre/probiotic/synbiotic approaches in the gut or aerosol in the airways.
Carbohydrate/Enzyme biotech companies
The outcomes of this work will be of direct interest to companies commercializing novel glycoenzymes (e.g. trans-sialidases) (e.g. Prozomix, Megazyme, Nzytech) and those developing effective bioassays, glycosidase inhibitors, and carbohydrate-based diagnostics and therapeutics (e.g. Ludger; Iceni Diagnosis), or speciality carbohydrates such as sialylated oligosaccharides (e.g. Glycom, Carbosynth, Inbiose) for potential application as neutraceutical, pharmaceutical and cosmetic ingredients.
Biopharmaceutical/drug companies
The research may also be of interest to biopharmaceutical companies (e.g. GlaxoSmithKline) developing novel sialidase (or neuraminidase) inhibitors incl. Influenza neuraminidase inhibitors.
Food and Healthcare companies (Probiotics/Microbiome)
This research may also be of interest to companies interested in modulating the gut microbiome via pro/prebiotic approaches (e.g. Danone, Nestle, Yakult) but also an increasing number of biotech startups operating in the emerging gut microbiome space (e.g. MicroBiome Therapeutics, Enterome Bioscience).
Early career researcher
This project will provide a unique training opportunity for a post-doctoral scientist to work in a multidisciplinary environment spanning research Labs at IFR and UEA (BIO and ENV). There will also be opportunities for undergraduate students (from UEA) and visiting scientists to gain research experience through short-term placements. The PDRA will receive expert training in anaerobic microbiology, heterologous expression, carbohydrate biosynthesis and analysis (HPLC, MS- and NMR-based methods), enzymatic assays, bioinformatics (TGAC) and statistical analyses. The techniques are well-established and there is considerable expertise in conducting research on glycobiology and gut microbiology. There will be opportunities to collaborate with chemists and structural biologists. The PDRA will benefit from the established international network of academic and industrial collaborations of the NRP Labs.
Organisations
- Quadram Institute (Lead Research Organisation)
- UNIVERSITY OF OXFORD (Collaboration)
- University of California (Collaboration)
- Azienda Ospedaliera Universitaria Seconda Università di Napoli (Collaboration)
- Newcastle University (Collaboration)
- Hannover Medical School (Collaboration)
- UNIVERSITY OF YORK (Collaboration)
- Utrecht University (Collaboration)
- DIAMOND LIGHT SOURCE (Collaboration)
- University of East Anglia (Collaboration)
Publications
Bell A
(2023)
Correction: Biochemical and structural basis of sialic acid utilization by gut microbes.
in The Journal of biological chemistry
Bell A
(2019)
Elucidation of a sialic acid metabolism pathway in mucus-foraging Ruminococcus gnavus unravels mechanisms of bacterial adaptation to the gut.
in Nature microbiology
Bell A
(2020)
Uncovering a novel molecular mechanism for scavenging sialic acids in bacteria.
in The Journal of biological chemistry
Bell A
(2019)
A special sugar: how sialic acid impacts on metabolism, health and disease
in Microbiology Today
Bell A
(2021)
Mucosal glycan degradation of the host by the gut microbiota.
in Glycobiology
Bell A
(2023)
Biochemical and structural basis of sialic acid utilization by gut microbes.
in The Journal of biological chemistry
Bell A.
(2019)
A special sugar: How sialic acid impacts on metabolism, health and disease
in Microbiology Today
Coletto E
(2022)
The role of the mucin-glycan foraging Ruminococcus gnavus in the communication between the gut and the brain.
in Gut microbes
Crost EH
(2023)
Ruminococcus gnavus: friend or foe for human health.
in FEMS microbiology reviews
Juge N
(2019)
Glycobiology of Host-Microbe Interactions in the Gut.
Description | The gastrointestinal (GI) tract is heavily colonized with bacteria (gut microbiota) which play a vital role in human health. We provided biochemical evidence for the adaptation of prevalent members of the gut microbial community to the intestinal mucus niche in heath and disease. We have unravelled a new metabolic pathway for sialic acid utilisation by gut bacteria. We showed that this pathway was required for colonisation and spatial adaptation in the gut. |
Exploitation Route | This mechanistic knowledge can be used for the development of novel biomarkers of disease and strategies to modulate the mucus-associated microbiome. |
Sectors | Pharmaceuticals and Medical Biotechnology |
URL | https://quadram.ac.uk/sialic-acid-catabolism-in-microbiome-bacteria/ |
Description | A patent application has been filed |
Sector | Pharmaceuticals and Medical Biotechnology |
Impact Types | Societal |
Description | BBSRC ITAS International Travel Award Scheme |
Amount | £3,000 (GBP) |
Organisation | Quadram Institute Bioscience |
Sector | Academic/University |
Country | United Kingdom |
Start | 09/2021 |
End | 10/2021 |
Description | Development of multi-step enzymatic routes for the synthesis of sialic acid derivatives |
Amount | £103,000 (GBP) |
Funding ID | IBCarb-PoC-0315-009 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 09/2015 |
End | 05/2016 |
Description | Norwich Research Park Bioscience Doctoral Training Partnership |
Amount | £100,000 (GBP) |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 09/2015 |
End | 09/2019 |
Description | Norwich Research Park Bioscience Doctoral Training Partnership |
Amount | £100,000 (GBP) |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 09/2016 |
End | 09/2020 |
Description | Training interdisciplinary glycoscientists to get a molecular- level grip on glycocodes at the human mucosa-microbiota |
Amount | £466,300 (GBP) |
Funding ID | 814102 |
Organisation | European Commission |
Sector | Public |
Country | European Union (EU) |
Start | 01/2019 |
End | 12/2022 |
Title | DEEP-STD NMR |
Description | Our collaboration with Jesus Angulo at UEA led to the development of a new way of analysing how drugs interact with molecules throough adaptation of a technique known as ligand-based Nuclear Magnetic Resonance (NMR) spectroscopy |
Type Of Material | Technology assay or reagent |
Year Produced | 2017 |
Provided To Others? | Yes |
Impact | This method could to lead to stronger and more selective drug candidates. |
URL | https://quadram.ac.uk/completing-drug-design-jigsaw/ |
Title | LC-MS method for analysis of 2,7-anhydro-Neu5Ac |
Description | This method allows to separate and quantify 2,7-anhydro-Neu5Ac. |
Type Of Material | Technology assay or reagent |
Year Produced | 2024 |
Provided To Others? | No |
Impact | This method allows to determine the level of this sialic acid derivative (2,7-anhydro-Neu5Ac) in gut content in a specific and quantifiable manner, which can be distinguished from other sialic acid forms such as Neu5Ac. |
Title | Membrane-enclosed multienzyme (MEME) synthesis of 2,7-anhydro-sialic acid derivatives. |
Description | A facile one-pot two-enzyme approach has been established for the synthesis of 2,7-anhydro-sialic acid derivatives including those containing different sialic acid forms such as Neu5Ac and N-glycolylneuraminic acid (Neu5Gc). This synthetic method, which is based on a membrane-enclosed enzymatic synthesis, can be performed on a preparative scale. Using fetuin as a substrate, high-yield and cost-effective production of 2,7-anhydro-Neu5Ac was obtained to high-purity. This method was also applied to the synthesis of 2,7-anhydro-Neu5Gc. The membrane-enclosed multienzyme (MEME) strategy reported here provides an efficient approach to produce a variety of sialic acid derivatives. |
Type Of Material | Technology assay or reagent |
Year Produced | 2017 |
Provided To Others? | Yes |
Impact | The method allowed to produce 2,7-anhydro-sialic acid derivatives (not commercially available) in amount and purity allowing further mechanistic studies and exploring applications in the health sector |
Description | Carbohydrate synthesis |
Organisation | University of California |
Country | United States |
Sector | Academic/University |
PI Contribution | Utilised carbohydrates provided by collaborator in scientific research projects |
Collaborator Contribution | Provided bespoke carbohydrates upon request |
Impact | Carbohydr Res. 2017 Nov 8;451:110-117. doi: 10.1016/j.carres.2017.08.008; Nat Commun. 2017 Dec 19;8(1):2196. doi: 10.1038/s41467-017-02109-8. |
Start Year | 2015 |
Description | Chemical glycobiology |
Organisation | Utrecht University |
Country | Netherlands |
Sector | Academic/University |
PI Contribution | Contributed to successful multidisciplinary European Training Network Sweetcrosstalk proposal Supervising tow ESRs on the project WP leader |
Collaborator Contribution | Coordinator of ITN Host of one of my ESRs |
Impact | Chemistry, Glycobiology, Microbiology |
Start Year | 2018 |
Description | Microbial polysaccharides |
Organisation | Azienda Ospedaliera Universitaria Seconda Università di Napoli |
Country | Italy |
Sector | Hospitals |
PI Contribution | Provided collaborator with bacterial samples to be analyses |
Collaborator Contribution | Purified bacterial cell surface polysaccharides and analysed glycosylation chemical structures |
Impact | Joint Abstract describing the collaborative work to Conference |
Start Year | 2018 |
Description | Molecular Microbiology |
Organisation | Newcastle University |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Provided material (2,7-anhydro-Neu5Ac) |
Collaborator Contribution | Received engineered plasmids |
Impact | Joint publications |
Start Year | 2022 |
Description | STD-NMR |
Organisation | University of East Anglia |
Department | Schools of Pharmacy and Medicine UEA |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | We provided proteins and ligands for analysis by STD NMR to complement some of our data on mechanisms of host-bacteria interactions. This collaboration resulted in high impact joint publications led by QIB (Proc Natl Acad Sci U S A. 2018 pii: 201715016; Nat Commun. 2017 ;8(1):2196) |
Collaborator Contribution | STD- NMR analysis of proteins and ligands we provided. Some of this work led to the development of DEEP STD NMR, leading to a joint publication led by UEA (Angew Chem Int Ed Engl. 2017 56:15289-15293). |
Impact | Proc Natl Acad Sci U S A. 2018 pii: 201715016; Nat Commun. 2017 ;8(1):2196; Angew Chem Int Ed Engl. 2017 56:15289-15293 |
Start Year | 2014 |
Description | Sialic acid recognition |
Organisation | University of York |
Department | Department of Biology |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Initiated collaboration on sialic acid transport and metabolism in bacteria |
Collaborator Contribution | Provided materials and contributed to data analysis |
Impact | Scientific publications |
Start Year | 2018 |
Description | Sialobiology |
Organisation | Hannover Medical School |
Country | Germany |
Sector | Academic/University |
PI Contribution | Presented unpublished data to collaborator |
Collaborator Contribution | Feedback on data |
Impact | Manuscript in preparation |
Start Year | 2019 |
Description | Structural biology |
Organisation | University of Oxford |
Department | Oxford Hub |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Identified and functionally characterised a novel enzyme activity in gut bacteria |
Collaborator Contribution | Crystallisation of metabolic enzyme involved in carbohydrate utilisation by bacteria |
Impact | Manuscript in preparation 3D Structure |
Start Year | 2019 |
Description | Synchrotron Oxford |
Organisation | Diamond Light Source |
Country | United Kingdom |
Sector | Private |
PI Contribution | Provided collaborator with proteins and ligands for X-ray crystallography and cryo-EM |
Collaborator Contribution | X-ray crystallography of proteins free and in complex |
Impact | Nat Commun. 2017 Dec 19;8(1):2196. doi: 10.1038/s41467-017-02109-8. |
Start Year | 2016 |
Description | 4th Annual European Microbiome Congress |
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 | Attendance to 4th Annual European Microbiome Congress. This Conference has a high representation from the Industry: Pharmaceutical companies and Biotechnology companies and provided an excellent opportunity to make contact and discuss work relevant to the Institute Strategic Programmes. The PROMOTING WOMEN IN SCIENCE lunch session was inspiring. |
Year(s) Of Engagement Activity | 2018 |
Description | External presentation (London School of Hygiene & Tropical Medicine) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Postgraduate students |
Results and Impact | The purpose of the presentation was to explore ground for scientific collaboration. |
Year(s) Of Engagement Activity | 2019 |