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Down the Rabbit Hole: Foodomics – Olivia McAuliffe

Olivia McAuliffe is a Principal Scientist at the Teagasc Food Research Centre in Ireland. Her team explores the genetics and genomics of food cultures and how new technologies can be applied within the biotechnology/food industry. McAuliffe also has a particular interest in bacteriophages and the development of therapeutic uses of these phages to target multi-drug resistant pathogens.

Please note the transcript has been edited for brevity and clarity.

FLG: Hello, everybody, and hello, Olivia, thank you for joining me as we go down the rabbit hole and explore some of the more niche and unusual aspects of where genomics is being applied. Today, we will be discussing foodomics. Before we start, Olivia, could you introduce yourself and explain what you do.

Olivia: Thank you, Shannon, pleasure to be here today. I’m a principal scientist and I work for the Teagasc Food Research Centre which is in Cork in Ireland. Teagasc is the Irish agriculture food development authority, so we are the national body providing research, advisory and training services to the agriculture and food industry and the wider rural community. Our mission is to support science-based research and innovation in the agri-food sector and in the wider economy.  There are several research programmes in Teagasc, and I work in the food programme. Our remit in the food programme is to look at food, food components and food-based microorganisms, in terms of our health and wellbeing, in terms of quality and safety of food that is produced, and in terms of the processes that are required to formulate and produce that food. We work extensively with the food industry, both here in Ireland and abroad, to address some of the challenges around those issues.

Myself, my research programme focuses mainly on food-based microorganisms and their role in sustainable food systems. We apply genomics and other technologies to understand their role in food in terms of the beneficial microorganisms, and then the impact of the not so beneficial microorganisms – the ones that cause foodborne disease, for example. In more recent times, we’re looking at how we can further exploit some of these microorganisms to make our food system more sustainable. For example, looking at conversion of waste streams and bio-based products using microorganisms as a tool to do that. So that’s where I work and that’s what I do!

FLG: Foodomics is an emerging field – for those who don’t know, would you be able to briefly delve into what it is?

Olivia: Foodomics is a term that was first coined in 2009 and what it is, really, is the application of omics technologies to the science of food. So, whether that be genomics, proteomics, metabolomics, transcriptomics. It is the application and integration of those technologies in the food and nutrition domains. It’s a multidisciplinary approach to the problems of connecting food components – the food, the diet, the individual (the host/ourselves) and our health, and the diseases that are driven by food. Mainly looking at it through a different lens, a multidisciplinary lens, bringing all of the omics technologies together to tackle the issues that are in the food system.

FLG: What is the importance of studying food?

Olivia: Food and the agri-food sector is a massive driver of our health, our social and economic wellbeing and it’s worth about 8 trillion euros to the global economy. It employs about 20% of the world’s population – many of those people are working in developing countries, so it is crucially important to their economy. The agri-food sector is a key sector for health and prosperity of all of us. But the sector is facing massive global challenges at the moment to the production of nutritious and safe and sustainable foods. So, the study of food, how we interact with that food and how we produce it has never been more important.

FLG: How has the field changed over the past few decades?

Olivia: I think we are at a tipping point, and I think many people who work in the food sector can see that as well. I mean, with the impact of climate change and environmental threats. The agri-food sector is responsible for about a third of greenhouse gas emissions. We have issues around the availability of sustainable land and water for food production. Maybe the biggest one is the world’s changing demographic. At present, we have a population of almost 8 billion people. 2 billion of those people are hungry, another 2 billion of those people have what is called hidden hunger (deficient in micronutrients that are essential for development) and you’ve another 2 billion people who are either overweight or obese. So, the system looks to be broken and about a third of the food that we produce is never eaten, so it goes to waste. So, how can we fix that system with a growing population?

By 2050, the population is expected to be 10 billion. We will have to produce 70% more food, but we’ll have to do that with a hugely decreased environmental footprint. So, the challenges ahead are enormous. And actually, it’s a really important year for the food system because the UN has called a Food System Summit that will happen in September of this year, and at that summit each nation will have to present how we’re going to fix this system, how we are going to change the current system that is used for food production to meet the UN’s Sustainable Development Goals. And the summit has been called because we seem to be going off track in order to try and address those challenges. So right across the sector, transformational change is needed and it’s going to take everybody in the system – all the way from primary producers right up to the consumer – to change the way we do things in order to fix it.

FLG: What are some of the key areas of food science that you are focussing on?

Olivia: There are a number of areas that the science of genomics has been applied to in food science. Like in every scientific field, the application of genomics has just revolutionised our understanding of what’s going on in that field. It has already brought huge economic and societal gains through better healthcare and improving food quality and safety. But I suppose some of the particular problems that genomics has been applied to successfully at this point, would be things in regards to food safety. So, food outbreak investigations as a result of eating contaminated food products), also in terms of food fraud and traceability. Antimicrobial resistance, which is another massive global challenge which I didn’t mention earlier, but the possibility of disseminating antimicrobial resistance through the food chain is an issue that genomics has been able to facilitate – understanding more about that). The impact of genetically modified organisms in the food chain – we have this new concept of genome editing, which has come about through genomics. And then the study of the interaction of the host (ourselves) and our microbiome and our diet, and how that is driving health and disease. So, they are some of the issues that genomics is helping to tackle at the moment.

FLG: How can studying the way food interacts with our genes and our gut microbiome help in the identification of potential therapies?

Olivia: I suppose the concept of using the diet to drive our health is not a new one. But what is becoming more evident now through the use of genomic is, how there’s an intermediary. It’s not just food for the host; it’s food for the microbiome. And a diverse, resilient microbiome we now know is essential to our health. So, we can use food to drive that diversity of population through the use of prebiotics, which is supplying sugars to the microbiome. Depending on the type of sugar that you provide, you will have a different composition of your microbiome and that could be good or bad. We can also use probiotics which are live organisms. We all know about the Actimels and the different types of probiotic drinks that you can have, yoghurt products or you can take them as a supplement, and these are, in some cases, assisting to replenish the microbiome. The study of probiotics has been driven a lot by genomics because being able to sequence the genomes of these organisms has really helped us to understand what it is about them that is improving our health.

We also have the whole concept of microbiome transplantation, so can you replace somebody’s microbiome with a brand new one that is going to help in resetting that person’s health journey. There’s lots of different ways of deployment of those strategies, from either the consumption of food and supplements, or more drug-like interventions, like specific therapeutic uses of these probiotics or microbiome transplants or whatever. That’s an area where genomics has revolutionised our understanding of the relationship between the host, the diet (the food that we consume) and our microbiome.

FLG: Could there be a time where all of our food is engineered to give us the right nutrients and the right microbes et cetera, or this too futuristic?

Olivia: I suppose that is the concept of personalised nutrition, really. What we’re used to is seeing nutrition guidelines for the population or for individual groups of people, whereas as what you’re talking about is personalised nutrition – tailoring it to your unique requirements. For example, the nutrition requirements of a young male who might be obese are going to be completely different to an older woman who has diabetes. So, we want to look at those specific individual needs and tailor diets and biotherapies (like we were talking about probiotics or microbiome transplantation) to those individuals. That can be a simple approach through incorporation of a probiotic and prebiotic or bioactive molecule into a food, or it becomes a little bit more complicated when you’re trying to deliver something that’s going to either modulate the immune system, or it’s going to impact the composition of the microbiome, or it’s going to target a particular pathogenic organism that might be present in that individual’s gastrointestinal tract. It’s not an easy fix. It’s not an easy thing to do because you need to deliver that particular modulator into the person’s diet, but certainly this is no longer science fiction. We’re at the stage where personalised nutrition and personal medicine is becoming a reality because we have technology like genomics in order to understand those interactions better.

FLG: You mentioned how omic technologies are being used in food safety. What research have you been exploring?

Olivia: Food safety is one of the areas which has really benefited from the use of genomics. When I talk about food safety I’m talking about foodborne disease, so disease that is caused by the consumption of contaminated food. There are about 600 million cases of foodborne disease every year – it’s staggering when you think about it. When we eat food, it’s for health benefits. We don’t think too much about the fact that it could make us sick, but there’s lots of cases of foodborne disease. Prior to the development of genomics there were other molecular methods that were used to study the epidemiology of food outbreaks, things like multi-locus sequence typing, polyacrylamide gel electrophoresis. These were the gold standard methods for typing the bacteria that were causing foodborne disease. They were sufficient because we didn’t have anything else, but their discriminatory power was quite limited. The problem there is tracking back to the food. If you become sick because you eat a contaminated food product and you’re not the only one who becomes sick in your household or in your bubble or wherever, then you have an outbreak. If you have an outbreak, you need to be able to track back to where that food came from and is there other people who are going to be impacted by consuming this food. Whole genome sequencing has provided us with a resource to do that – source tracking – finding out what food product is the cause of the outbreak, and this has really transformed our ability to find the source of outbreaks. It’s now being used by regulatory and public health agencies. This was really driven by the US Food and Drug Administration, and it’s now being applied right around the globe, particularly in more developed countries because the technology is expensive.

But we could see in a recent outbreak in South Africa of Listeriosis. Listeriosis is a disease which is caused by an organism called Listeria monocytogenes. It is associated with ready-to-eat foods. If you cook a product, Listeria dies in the cooking process. But it is associated with things that we buy, put in our refrigerators and directly eat from the fridge. So, things like deli meats, coleslaw and salad. There was an outbreak in South Africa in 2017 into early 2018 associated with a deli meat, like a baloney meat. It was the largest outbreak of Listeriosis recorded to date. But they were able to track back to that food processing plant relatively quickly with the help of whole genome sequencing. Perhaps without it, the situation would have been a lot more dire. So being able to close down the implicated factory in quite a rapid manner through the use of whole genome sequencing really prevented that problem becoming a lot worse and contained it so that it didn’t spiral out of control. In our research, what we’re doing is we’re using genomics to look at this organism, Listeria in particular. It’s a rare disease but the fatality rate is quite high – so it’s between 20 and 30% – and there are a number of vulnerable groups, like the elderly and the young and immunocompromised people and pregnant women. So, there are a number of distinct vulnerable groups.

It is an interesting organism to study and what we’re looking at is, we’re using genomics and trying to combine that with looking at the phenotype of the organism (the behaviour of the organism in the food processing plant, in the food and in clinical settings) and trying to connect the dots between what we see in the genome and how the organism behaves so that we can predict what the organism might do in a food product or in a food processing plant. And then we can use that information to try and prevent the contamination from happening in the first place.

FLG: What are the challenges of using these technologies within low-income countries?

Olivia: There are barriers, for sure, to implementing these types of technologies in low- and middle-income countries. There are costs associated with it – costs of the equipment, the cost of the consumables, the costs of training personnel. The most important thing for these developing countries is that there’s a surveillance system in the first place. Whatever type of technology that you’re using, the surveillance is the most important thing. The higher-end technology can come later, but once there’s a surveillance system in place. They do use the older technology that we’re moving away from more in the Western world now, but that does facilitate the type of source tracking and surveillance that I talked about as well – it just might take a little bit longer. I guess if those systems are in place first, you’re starting from a good position. And the cost of sequencing is decreasing – it is decreasing year on year – and also the equipment necessary to facilitate this type of sequencing is becoming quite science fiction. These miniature handheld sequencing devices that you can now go in and take your samples on site – these types of devices will help with the implementation of these sequencing technologies in low- and middle-income countries. So, the outlay is not what it might have been even five or ten years ago in terms of implementation. So, while there are still obstacles, it is becoming more of a reality. And as we move towards a more genomics approach to the epidemiology of foodborne outbreaks, the key thing is that surveillance is in place first, no matter how you’re doing that, and then the high-end technology can come later.

FLG: Antimicrobial resistance is a major global crisis. How can omics technologies be used to detect AMR bacteria in the food chain?

Olivia: There’s certainly growing concern over AMR transmission in the food chain. Food can become contaminated with AMR bacteria during primary production and at all other stages along the chain. So again, monitoring and surveillance is critical, and the classic AMR surveillance has been done again through phenotypes, characterising the isolates in terms of their behaviour, and then later we moved to using molecular methods, like PCR for detection of AMR genes. But again, omics technologies have transformed how we look at these organisms. So whole genome sequencing of organisms that are expressing antimicrobial resistance. Then subsequently, and maybe more importantly, is the use of metagenomics, which is instrumental in studying the prevalence and dissemination of these organisms in the food chain. A metagenomics approach has the advantage of getting a snapshot of the entire bacterial community, so what you’re looking at there are the organisms that you can culture, but you are also looking at the organisms that you can’t culture in the laboratory. This is what metagenomics has helped us to do. You’re looking at the entire population, the things that you can work within the laboratory and the things you can’t work with in the laboratory. That gives you a much more broader view of what’s going on. Metagenomics allows us to study what is called the resistome, which is the entire repertoire of genes in a community that are involved in resistance to antimicrobials, and this is really helping us to improve our ability to monitor and track these organisms as they move through the food chain, because dissemination through the food chain is going to have to be tackled in order to address the issue of AMR.

FLG: How does your research on food safety and AMR inform the rest of the food chain?

Olivia: I suppose it is multidisciplinary – it’s not just microbiologists. We are working with food technologists, food processors, bioinformaticians – right across the disciplines. That is what has changed about science of food and science of food technology over the last decade. It’s bringing together different disciplines to try and tackle the problems that are there because it’s not just one. If you go from farm to fork, you have lots of different actors, lots of different activities all the way along that food chain and different expertise are required right across the spectrum. Genomics can be applied to any area of that, but you also need the experts who work with the primary producers, you need the experts who work with food processors, you need the experts who work at retail and then packaging and processing for the consumer. It’s a multi-actor activity now, food science, and one particular expertise or discipline is not going to solve the issues we have at the moment.

FLG: Another area of research you explore is characterisation of bacteriophages – would you be able to go into this into a bit more detail?

Olivia: Sure! I like to talk about it because for a long-time people were going, ‘Bacteriophages?! What are they?’ And of course, we have talked about nothing but viruses for the last 15 months of our lives, so the fact that viruses are becoming interesting for people again makes me very excited. A bacteriophage is a virus that infects and destroys bacterial cells only. We interact with viruses every day. There are good ones, as well as the bad ones, and these viruses are specific for bacterial cells, so they don’t do us any harm whatsoever! What they do do, is they control the bacterial populations in the environment, and that is really important because we don’t want any one specific bacteria getting out of hand. So, these bacteriophages are the natural predators of bacteria, and they keep the microbial systems in different environments in check. And actually, if you are talking about genomics, the first full genome sequence was of a bacteriophage – all 5,000 base pairs of it back in 1977, sequenced by Fred Sanger and his team. And people may be familiar with Sanger sequencing – his name became synonymous with that, and he won the Nobel Prize for his sequencing of a 5,000 base pair bacteriophage.

But I suppose for a long time the science of bacteriophages concentrated on bacteriophages as a problem because they tend to be a problem in the dairy industry. So, wherever you have got large volumes of bacteria being grown and if you have a bacteriophage or virus getting into that situation, it can kill the bacteria there and then cause problems in dairy industry. So, in the fermented diary industry where they grow large volumes of bacteria for the production of cheese or yoghurt or other fermented products, if you have a virus in that situation, it can be detrimental to the production process. So, we were looking to control the bacteriophages when I first joined Teagasc. It wasn’t a new concept, actually, it was quite an old concept, the concept of bacteriophage therapy (using bacteriophages to kill pathogenic bacteria), and that had been something that had been done at the discovery of bacteriophages right back in the early 1900s. But with the advent of antibiotics, that research went off a cliff. People were like, ‘We have solved the problem of pathogenic bacteria. We now have antimicrobials or antibiotics. We don’t need to study phage therapy anymore’. But of course, we know how that story ended and we are here now with a huge antibiotic resistance problem, and perhaps phages are the way out of the problem!

In my group, we have been looking at using bacteriophages to target and kill pathogenic bacteria and there are multiple ways that you can do that. You can use the whole phage to kill the pathogenic bacteria of interest. But we’ve also been using genomics to look at bacteriophages and to identify within their genomes specific enzymes that can be used and produced recombinantly to kill the bacteria, so you’re no longer dealing with the whole phage, you are dealing with an enzyme that the phage produces which can be used to kill bacteria. So, similar to antibiotics. You’re recombinantly producing an enzyme that can target certain problematic bacteria. We have been applying genomic studies of bacteriophages for a long time and there’s been an awful lot of good science done. The regulation in regards to using those agents to treat bacterial disease is a little bit behind the science, and I think that we are at a point now where the issue of antimicrobial resistance is so real that we need to start looking at all options that are out there as alternatives. And bacteriophages could certainly be one!

FLG: How can advanced genome engineering technologies, like CRISPR, improve this field of research?

Olivia: CRISPR and genome editing could become somewhat of a game changer in the agri-food sector and it really has huge potential to become the future of crop improvement and also livestock breeding. For people who may not be familiar with it, we have heard an awful lot about it in recent years. It is adding, deleting or altering the genome in a very site-specific fashion. But unlike genetic modification, there’s no foreign DNA introduced. I suppose the supporters of it, or the scientists who work on it, would say these are changes that would happen naturally in the environment anyway; we’re just speeding up the process. They would say it is distinct from genetic modification. There’s been a lot of research in recent times in harnessing this technology to improve agronomical traits in plants while maintaining their beneficial characteristics. Whether that be larger grain size in rice or more drought resistant plants, improving the eating quality of certain products, producing non-waxy variants of certain corn plants, producing seedless tomatoes. So really targeting specific things about the plant and improving that, while maintaining all the other beneficial characteristics.

It’s also been looked at in the laboratory in terms of what we talked about earlier with probiotics, so looking at using genome editing to modify these organisms so that they can more readily modulate the immune system, so that they can produce antimicrobials that target pathogens, for example, and that can modulate the microflora in a specific manner. So, it is being very much applied in the laboratory, but there are issues around applying this technology and rolling it out because in some cases, it’s not seen as anything other than genetic modification and obviously there are issues with that in the food system.

FLG: How do you think this field will evolve over the next decade? What are some of the remaining challenges?

Olivia: I think looking forward one of the main challenges for the food sector is, how do we focus on improving the sustainability of the food system. There’s a lot of talk now around the circular bioeconomy, so how can we sustainably produce food by extracting maximum value from anything that is produced, and any resource that comes into the system is utilised to its maximum potential and its maximum value. So, moving away from an economy that practises take, make and waste to the principle of reduce, reuse and recycle. The food system is another system that needs to move in that direction. Right across national policies now, these types of approaches are being implemented, and genomics and other sciences will certainly be central to driving that. But as I mentioned already, it will be about working with researchers from other disciplines, using their unique perspectives and expertise to tackle some of these issues that I’m talking about. We need the agricultural scientists, we need the nutritionists, we need the genetic engineers, we need the biotechnologists – we need everybody to come together and come up with innovative solutions to some of these problems.

I suppose it has been noted before that the food sector tends to be relatively slow to harness new technologies because the consumer wants what it wants, and you don’t try to interfere with something that’s working for you. I think we’ve done it in the past, we’ve gone from a situation where people understand the difference between good bacteria and bad bacteria and how taking in good bacteria can influence your health. Can we go down the same road with educating people to be aware of the fact that there are good viruses and bad viruses? It’s probably not the best time to try to do that but over time, we may be able to convince people that that’s something that is beneficial for them. Consumers are becoming a lot more educated now as well. We have people looking for smart labelling. They want to be able to scan their food product on their smartphone and see what are the benefits for me of eating this food. But not only that, what is the environmental impact of the production of this product, the sustainability of the process that put this food on my supermarket shelf. And this is probably going to be the difference for food processors in the future – how can they prove to the consumer that they are producing their products in a sustainable and environmentally friendly way.

FLG: Thank you so much for joining me today, Olivia, it has been really interesting and I’m excited to see how this field evolve, especially bacteriophages!

Olivia: Great!

FLG: I am now a fan of bacteriophages!

Olivia: We should all be fans of bacteriophages. It’s a tough sell at the moment where virus is a dirty word, but I certainly think that in the future, we will be thankful for their presence.

FLG: Thank you!