The Human Microbiome: A New Frontier in Health

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Microbiome expands the genetic and functional capacity of its human host. Susan Lynch explains that human microbiome develops early in life and that gut microbes shape immune function and relate to disease outcomes in childhood. She also explores next-generation microbiome therapeutics and research. Recorded on 11/07/2019.

👍︎︎ 1 👤︎︎ u/easilypersuadedsquid 📅︎︎ Dec 25 2019 🗫︎ replies

This is really a very good lecture. You should definitely watch it.

👍︎︎ 1 👤︎︎ u/easilypersuadedsquid 📅︎︎ Jan 01 2020 🗫︎ replies
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(upbeat music) - I'm thrilled to be with you tonight to share with you a relatively new and I think incredibly exciting field of research that's really changing our view of human biology. The field of human microbiome research. And that really describes studying the intense diverse communities of bacteria fungi and viruses that live in and on the human body and understanding how they shape our health. So what will we cover tonight? Well, first things first. How do you study entire communities of microbes? What tools do we have and how do we understand not just who's there but what they're doing and how they're interacting with the human host. And we'll go through a quick whirlwind of the human microbiome. Human microbiome 101. And then I wanna shift into some of the work that we've been doing in leveraging the very early life gut microbiome to understand an airway disease that occurs years later in childhood. So not your typical thinking inside the box on this one. And how we can use the microbiome not just to predict allergic asthma development but to understand why it develops in these children in very early life and to develop new therapeutics to intervene early to prevent disease development. And then I wanna give you a quick rundown of what's next. What is in the future. What's the crystal ball for this field, what are we developing here at UCSF and beyond to leverage findings in this field to really develop what we see as a new field of microbiome medicine. And so when I begin my lectures, I like to begin at the beginning. The very very beginning: the birth of the planets. And point out that the first and most successful organisms on the planet are microbes. They're bacteria. They have been around the longest. They are the most successful. They're also the most numerous, the most diverse and ubiquitous. Everywhere we look on this planet we can find microbes. They have evolved and adapted to live in the most extreme of environments. That can be everything from an acid mine to the incredible pressures at the bottom of the ocean to incredible extremes of heat and chemical exposure for example. So they're a depth. They can live in the most extreme environments. And as I said, they are everywhere. So we as well as every other biological entity on this planet have evolved in a microbial soup. And in fact we haven't just evolved in a microbial soup, we've co-evolved with microbes. They live in and on us and we actually rely on them for functions that we ourselves do not encode in the human genome. But how have we studied microbiology? Well, we've taken a very reductionist view traditionally. What we've traditionally done is taken microbes out of their environment, grown them under feast conditions in laboratory media by themselves and studied what they do. And nothing could be further from the truth of how these microbes exist. They're actually quite social. They live like us in diverse communities. They communicate with one another, they use small molecules to sense who's in their neighborhood and respond those microbes that are in their neighborhood. So how do we get at these organisms, many of which we've never cultured. We don't know how to grow them, we don't know what they eat, we don't know what they subsist on. We turn to molecular tools. So the kind of workhorse of the field of microbiome research is using DNA based methods to identify microbes without ever having to grow them or isolate them from a sample. We'll take a sample, we'll extract the DNA from it and remember that DNA comes from every microbial cell in that sample. There could be various different types of microbes and then one approach we have is really targeting specific genes like this one called the 16S ribosomal RNA gene. This is a gene that's only found in bacteria. It's not found in any higher organisms and it's a great biomarker gene for identifying which bacterium it came from because it has these regions in the gene that are really highly conserved across all known bacteria. So we use those highly conserved regions to kind of anchor an assay that we have to basically make copies of the region in between. And the regions in between those really conserved regions of the gene are what we call hyper variable. There the sequence varies. And it varies depending on which bacterium the gene came from. So we can make lots of copies of these genes and then sequence the hyper variable region to figure out who it came from. And in that way we can generate like what you would think of as a fingerprint which bacteria are there and in how much of each bacterium is there. What's the relative abundance. And this is really useful for comparing across very large cohorts of samples where we just wanna know who's there and how it differs, for example, in health and disease. We've got a similar tool for looking at fungi. There's a lot of various regions we can look at with the same type of technique but we tend to use this one called a interspacer region two. Again, we amplify that piece of the genome from fungi, sequence it and then we can tell which fungus it actually arose from and in that way look at fungal communities and how they're composed. Who's in that fungal community. But the tools for assessment of the microbiome have rapidly evolved and expanded in capacity over the last several years. And we now can, instead of just looking at a biomarker gene, actually take all of the DNA we extracted and sequence all of that DNA and then put those pieces back together basically reassembling the genomes of all of the microbes in that sample. And this is no small feat as you can imagine. I joke, although it's not really a joke, and I say it's like me handing you "War and peace" by Tolstoy in pieces and asking you to put it all back together in a legible form. That's the the computational capacity that we need. Is immense to do this job but something that we have developed very rapidly over the last several years. So while biomarker gene sequencing tells us who's there, shotgun metagenomics tells us the genes that these organisms encode and what they have the capacity to do. But we've pushed this field even further. We can also extract RNA from a sample. It's another type of nucleic acid. And it basically it's the transcription of those genes. So it's what is that the community of microbes actually transcribing off their genomes. Wow are they responding to the current conditions. And we can sequence those pools of extracted RNA by sequencing also and we call this meta transcriptomics. It gives us a snapshot into the genes that are being expressed at the time of sample collection by organisms in the microbiome. But what's even more exciting is that we can look even deeper. These are all next-generation sequencing based tools to look at microbiomes. We can also use mass spectrometry, the capacity to identify small molecules. And we can use this to look at protein pools produced by the microbiome to understand the proteins that they produce and that includes remember, all of the enzymes and catalytic functions of the microbiome. But what's nearest and dearest to my heart is metabolomics. Looking at the small molecules. Remember I said that that's how microbes communicate with each other. In fact, that's how cells communicate with each other irrespective of their microbial or host. And this for me is the lexicon that governs microbial-host human host interactions and this is where we think the next frontier and we're all already realizing the next frontier in this field really lies. So the application of these tools and in particular DNA based tools, has massively expanded our view of bacterial life on this planet. This is the tree of life. This is everything. We're down in one of the little branches down there on the bottom with the eukaryotes. These up here on the top are all bacteria. And this is a study that was published in 2016. Everything in purple are brand new bacteria that were identified in this study alone with molecular methods. So we have immensely diversified the bacterial tree of life and we suspect that this is also true for viruses and for fungi. We just need to catch up in developing the tools for those realms of microbial life. But what these tools have told us is that there is a much broader range of fungi and viruses. Particularly those that exist in the human body than we previously were led to believe based on culture-based approaches. And in total, the application of all of these tools to interrogate the microbiome has left us realizing that we're not alone. We are, in fact, super organisms. We're a conglomerate of microbial and mammalian cells that have co-evolved over time and we are colonized inside and out by microbes. This is just simply looking at microbial diversity across the surface of the skin. Anything in red is kind of higher diversity, in blue is regions where there's lower microbial diversity. This is looking with mass spectrometry at the molecules made by those microbes on the skin. And here you can see that even where there's regions for there's not so many microbes present, there's a huge biochemical diversity of molecules that are produced at those sites. Produced by the microbes, produced by the host cells in response to the microbes. There's a rich molecular lexicon occurring at these sites. That's simply the skin. And that's actually considered a very low microbial burden sites. We house the greatest burden and diversity of microbes in our gut. Particularly in the distal gut. And these microbes are not simply bystanders. These microbes influence how our gastrointestinal cells behave and function and respond to this microbial zoo in the lower gut. And I will say it's not just the lower gut. There are microbes obviously in the mouth and the whole way down through the GI tract. They differ at different sites along the GI tract. And we think that that's because of the prevailing conditions that differ. If you think about in the stomach, the pH is very low. in the lower gastrointestinal tract, there's very little oxygen there. These are strong selective pressures that drive the types of organisms that like to thrive in these distinct niches along the gastrointestinal tract. But I think what's really amazing is to think about how much our microbiome dwarfs our human genome in terms of genetic capacity and genes that it encodes. This is one study of European Asian and U.S. populations. Just over 1,200 fecal samples were sampled and examined using shotgun metagenomics. So looking at all of the microbes and all of the genes encoded by the microbiome in those 1,200 or so samples. And what staggering is, almost 10 million microbial genes were found just across those 1,200 or so individual fecal samples. I wanna let you think about that for a second. That is incredible. This is an ancillary microbial genome that we carry around with us. These genes are not silent. They're actively expressed. And we rely on these genes for things like digesting our dietary components, for digesting metabolizing our drugs, in fact and for informing and influencing our immune response. So these are an important part of our physiology. An important part of what makes us healthy or diseased. And to add the complexity that this is not just one type of microbiome that we have in one site. We develop our microbiome in early life. We are born with the very simple microbiome that we inherit from our mothers. It either arises in utero or is contributed to through the birthing process. Babies who are born through the vaginal canal, have a preponderance of lactobacillus species which are the dominant organisms in the female vaginal tract. Babies who come at the sunroof by cesarean section, end up quite frequently with organisms we find on the skin. Staphylococcus and streptococcus. Suggesting that very early life postnatal exposures influence those communities of microbes that are found in the very early gut. And as we proceed through very early life development, we now know that a whole range of factors influence and shape the types of microbes and activities of the gut microbiome. Things like early life nutrition, antimicrobial exposure, as I mentioned ceasarean section, really strongly influenced what type of microbes are there and how they're functioning. We continue to expand the diversity of bacteria that we have in the gut up until about three years of age. Around then the diversity looks like that of an adult but the functional genes in that microbiome at three years of age are quite different from that of a healthy adult. Throughout life we continue to shape our microbiomes. In fact, I view them as, in adulthood, as a history of your exposures in life. Things like pharmaceuticals, diet, infection, sex hormones, even environmental toxicants can serve as strong selective pressures on which microbes are present and what they're producing and therefore how they're interacting with the host. And to really reinforce this and add to the complexity, if we take a point in time not all microbiomes are equal. This is a study of the gut microbiome in developing and developed nations in adults in this case. Here in red and green we have gut microbiomes of Malawian and Amerindian populations. In blue we have the U.S. population. And basically each spot is a profile of what type of bacteria were in the gut microbiome of these individuals and how we work through this immense amount of data that we generate is we ask how similar is microbiome profile A to all of the other microbiome profiles in our cohort. And we calculate a distance. How similar is it, how close is it in terms of which microbes are there and what relative abundance, how much of them are there. And that's just a visualization of this distance calculation. So if we have two spots representing two gut microbiomes of individuals in these studies that are closely plotted beside one another, it means that those two gut microbiomes are very similar to one another. But what you can starkly see in this, is the U.S. gut microbiomes are very different from those of the Marindian and the Malawian population. And even though the Malawian and the Merindian populations are on two different continents, their gut microbiomes in these less developed nations are more like each other than they are like a U.S. population gut microbiome. To reinforce what we've done to our microbiomes in the U.S. this is just looking at the number of types of bacteria that are detected across these populations. We have severely reduced the breadth of diversity and the number of different types of bacteria in the U.S. population compared to the in less developed nations. And the really wonderful thing about this study, is we got indications why this might be happening. When the study examined with shotgun metagenomics looking at all the genes and the pathways and these microbiomes, what really differed between these populations, what was really striking, is that the adult population of Amerindian and Malawians were really enriched for alpha-amylases. So this is an enzyme that breaks down complex plant polysaccharides. So the diet in Malawi and in the Merindian population is predominantly a plant polysaccharide, a plant-based diet. In the U.S. population, we see huge enrichment of microbial metabolic pathways for processing simple sugars. Found in processed foods, as we all know. So at least one feature, one thing that we know is driving these differences in the gut microbiome across these populations is differences in diet in what we consume. And this was reinforced even more recently by Pete Turnbull who is a faculty member here. This was a really wonderful diet based study of 10 individuals. And what Peter did was he took those individuals and looked at how a plant-based or an animal-based diet may actually influence a healthy gut microbiome. And here we're just showing you the amount of fiber in their diet of these individuals before they started the study, then they got four days of a plant-based diet, the other participants got four days of an animal-based diet and as you would expect the fiber content with the plant-based diet or the plant polysaccharide content goes up quite high in an animal-based diet it's very low. Also, the fat intake is lower in the plant-based diet compared to the animal-based diet and the protein content is also dramatically different across these two diets and he could track that these key dietary component really shift with the introduction of either a plant-based diet or an animal-based diet. What was really striking is that when Peter calculated again the distance, how similar are the microbiomes of the individuals after they start their plant-based diet compared to before they started their plant-based diet, didn't really see much in the way of change. Plant-based diet doesn't really perturb the gut microbiome. However, in comparison, the animal-based diet introduction, really increased this distance. And what that tells us is that microbiome is very different from the microbiome that was there before the introduction of the plant-based diet. But it's not just about changing the composition of the microbiome that matters. What the study also showed is that you change the molecular output of the microbiome by changing the diet. And here we can see that two key short chain fatty-acids acetate and butyrate were significantly reduced in the animal-based diet versus the plant-based diet. And that makes sense because these are the products of microbial fermentation of plants, of fiber. And what's really critical is these short chain fatty acids are crucial energy sources for the cells that line the gut, they're antiproliferative and they're anti-inflammatory. And we think they have these activities because we've co-evolved with these microbes who traditionally have fermented our plant-based diets into these small molecules which quench inflammation and promote kind of health in the system. And so based on this, I'm sure you're not gonna be surprised that we're finding an ever-increasing range of diseases are related to perturbations to the microbiome. And things like the skin microbiome is perturbed in dermatological conditions like psoriasis for example. But what's really exciting is that we are now saying that conditions like obesity is also linked to gut microbiome perturbation. But what's most exciting for me, is that we're finding that conditions that are very difficult to treat and that we really don't have a handle on like depression and autism spectrum disorder are also linked to perturbations in the gut microbiome. Suggesting that the gut microbiome may actually influence remote organs. And there's a couple of really key seminal studies that have shown this. They've shown that perturbations in the gut microbiome are associated with autism spectrum disorder and also with cardiovascular disease. But importantly what these studies have shown, is that it's microbial metabolites, microbial products that are responsible for these disorders and much of this work has been done in mice with some follow-up work in humans. So it suggests that the gut is not like Vegas, what happens in the gut doesn't stay in the gut. It actually enters the circulation and these small molecules and perhaps there's some inklings even microbes themselves may actually translocate to other sites across the body and change the physiology of the organs there contributing to the health or disease of those remote organs but how do we really know that it's the gut microbiome that's responsible for this? Well, that evidence has come from some really elegant mouse studies. So in these studies, in this case that I'm showing you, the feces of obese individuals and lean individuals were transferred into germ-free mice. These are mice that have no existing microbiome. They're bred to lack a microbiome. They're not particularly healthy mice but they're bred to not have a microbiome. They're a wonderful vessel for studying how microbial introduction into kind of a pristine environment may shape the physiology of the host. And that's what these studies have shown us. Transfer of the obese microbiome into a germ-free mouse sets up an obesogenic microbiome in that animal and those animals gain weight at a much faster rate than that of animals who received the lean microbiome. Suggesting that the phenotype of the disease can be transferred from the patient by transferring the gut microbiome of that patient to a mouse. That's pretty incredible. That means that the microbiome is responsible in large part for obesity in this case. What's exciting is that it's not just obesity. This has also been shown for Kwashiorkor. This is a wasting disease with neurological deficits that can be quite prevalent in underdeveloped nations like Bangladesh for example. Same thing. Transfer of the Kwashiorkor gut microbiome or feces to germ-free mice induces wasting disease in those animals. More recently it's actually been shown for autism spectrum disorder. Feces from patients with ASD transferred into germ-free mice induce neuro behavior that is consistent with the symptomology of the disease . So again, we're finding multiple disease indications where we can recapitulate features of the disease in a mouse who receives the microbiome for the patients with the disorder. So what can we do? Well, we call it yellow soup for the soul. Fecal microbial transplant. I'm sure you've all heard of it. It's not new. I call it yellow soup for the soul because there are records in 5th century Chinese medicine, of producing yellow soup from feces as a treatment for gastrointestinal conditions. We've just recently rediscovered fecal microbial transplant. And what's very exciting is that it is essentially doing what we do in the mice but instead it's transferring the healthy gut microbiome from a healthy donor to the gut microbiome of a patient with a disease or condition or an infection to try and reconstitute the gut microbiome of the patient and treat the disease. So this has 92% efficacy in patients with Clostridium difficile infection. Antimicrobial treatment for Clostridium difficile is about 30% effective. And in this trial that used fecal microbial transplant to treat the Clostridium difficile infection, they actually stopped the trial early because it was really not, they could not treat the patients with this treatment because they were seeing 92% efficacy versus 30% in the vancomycin taper and microbial treated patients. It was unethical to continue the trial and not use this to treat patients. And we actually offer this at UCSF as a treatment for Clostridium difficile infection. It's also been used in a small pilot early study of children with autism spectrum disorder. It's about 18 or 19 children in the study. There they saw significant reductions in neurobehavioral symptomology in those children. In this case instead of a single treatment, where there's a colonoscopic delivery of the fecal slurry into the diseased gut. They did that initially but then they followed it up with a month of sustained microbial pressure in which the children actually consumed freeze-dried fecal capsules and that was sufficient, a month of treatment, to significantly reduce the neurobehavioral deficiencies in these patients. They've also recently followed up two years later with these children and this effect is sustained. And in fact, they've seen even greater improvements across this small cohort that has been treated. And so now this is under clinical trial in a much larger placebo controlled studies across the country as a potential treatment for autism spectrum disorder. We at UCSF have been looking at inflammatory bowel disease. I'm in the gastroenterology division. I can tell you that we looked at Crohn's disease and ulcerative colitis and fecal microbial transplant does not work for Crohn's disease. At least the way that we tried it with a single colonoscopy delivery. We had several adverse events and we shut down the study. And I think it's important for that message to get out equally as the 92% Clostridium difficile efficacy message. It's not equal. The microbiome is not the answer to all of our patients' ailments. And I think that it's important that we're cautious and that we are careful about how we implement this field and how we use this field to treat our patients. However, with an approach very similar to that, taken in the trial of autism spectrum disorder patients, we're now at about 40% response rate in our ulcerative colitis patients. And that's really exciting. You know our biologics are about maybe 20% efficacy and we try different biologics in patients to ask what will work for them. But we're seeing 40% response rate with fecal microbial transplant. We've got ideas how we can even enhance this even more and I'll talk a little bit about this a little later in the study. So for me, we're at a watershed moment in human biology. We've just discovered that we have this ancillary microbial genome that really influences our health that shapes how our cells work and influences our health status. And what I want to shift now is talking about how we leverage this field to tackle a disease that I know, probably everybody in the room knows somebody with asthma. Right, now in the U.S. we're at about 11% of our population diagnosed with the disease and it's growing. And you can see from this map this is a disease of westernized nations. This is a disease of lifestyle and environment. This is not necessarily a genetic disease in the typical sense. What I think most alarming for me is that the prevalence of this disease has increased most dramatically in the pediatric population. Children are disproportionately affected by allergic asthma which is the predominant form of asthma in this country. And for those maybe a little less familiar with the disease, it's characterized by a pretty specific immune dysfunction. Children with allergic asthma have far fewer of the specific type of T-cells called regulatory T-cells. They produce this molecule called IL-10. And you wanna think about these cells as putting the brakes on inflammation. We need them to dial down inflammation. So children with asthma have far fewer of these cells and instead they have much more of these ones. These are another type of T-cells called T2 cells. And they produce three other molecules called IL-4, IL-5, IL-13 and they ramp up inflammation. These children are also characterized by having very high concentrations of this antibody IgE in their circulation. So they're the Cardinal immune dysfunctional features of allergic asthma. Something to remember as we move through the rest of the presentation. I think what's also striking to me is that while we can treat our patients with corticosteroids, long-acting beta agonists, we have no cure. And that's what really drove me into this field and start thinking about very early life and what are the factors that influence disease development and could the microbiome be the canary in the coalmine for asthma and allergy development in childhood. And what drove me towards that idea was really the opportunity to stand on the shoulders of giants. There's many many studies that have tried to figure out the genesis or the developmental origins of allergy and asthma. So there's been lots of very large studies, birth cohort studies where babies are followed into childhood from birth. You know their early life exposures and you know whether they developed allergy or asthma years later in childhood. And these studies are really consistent in the factors that we know increase the risk of disease. There are things like formula-feeding, antimicrobial administration and cesarean section. And if those factors sound familiar, they are amongst the things I told you at the outset of this presentation, shaped the composition and the activities of the gut microbiome. On the flip side, decreased risk of allergies and asthma in childhood are associated with breastfeeding, with exposure to livestock and animals. And in fact we've shown in the inner-city environment to cats, mice and cockroaches. All vectors for microbes and they increase the microbial diversity and microbial exposure for babies in very early life. And we think that's important because we think the environment of the baby serves as the library of microbes that are available for accumulation into the gut microbiome and elsewhere as we develop our microbiome in that critical window of the first few years of life. But we were still, before we really launched into this field, interested in asking questions in models. Can the gut microbiome really impact the airways? Because no one had really shown that. And so to do this we did a pretty simple study in which we took mice and daily we fed them this lactobacillus species. We did that for a week before we sensitize the airways of the animals with cockroach antigens. So IT stands for intratracheal and CRA is cockroach antigen. So we expose the airways of these mice to an antigen that induces allergic inflammation. As a control group, we had animals who didn't receive the Lactobacillus johnsonii. And what we found was that in the animals that received the Lactobacillus johnsonii, you can see that they have significant we reduced IL-4, IL-5 and IL-13, the three molecules I told you that the the group of cells, the T-cells produce that promote allergic inflammation. And this was true whether we looked at the expression of these genes or the protein of these genes. And what was even more compelling is this is what the airways of these animals look like. These are the animals whose airways we've sensitized, who got no lactobacillus into the gut. Here are the airways of those that received the lactobacillus supplementation. The airspaces of these animals are absolutely pink and occluded with mucin. That pink staining stains mucin. So they are completely full of mucin. These are highly inflamed airways and this does not occur in the animals who received an oral lactobacillus supplementation. We began to start thinking about this. Is this just about allergy or is this really a more profound airway protection that occurs when we change the microbiome by introducing microbes into the gut. And so we asked the same question but here we didn't use allergen. Now we used respiratory syncytial virus or RSV. We think of that as an asthmagenic virus. Children who have an infection with RSV in the first few months of life that requires hospitalization, are significantly more likely to go on to develop asthma. It's kind of a red flag for asthma. And so we have this model in which here we used live lactobacillus johnsonii or heat-killed lactobacillus. Do we need a metabolically active microbe to engender protection in these animals. And PBS is just saline. That's the control in this study. And we know that when we infect these mice with RSV, they have this very predictable kind of infection dynamic and by day eight we can see profound pathology in the airways. And so what we found is that when we tested the airways of these animals for how responsive they were, only the animals that received the live lactobacillus johnsonii had significantly reduced reactive airways. And also they were the only animals that had significant reductions in allergic inflammatory markers and molecules in their airways. Again, IL-4, IL-5 and IL-13. So this told us that we needed a live microbe to actually confer protection in the airways. Which is what this is pointing out. But we began to think about how does this happen. What's actually happening before we get to that stage where we can see differences in airway pathology. And so we rolled back the timeline on this model and simply asked with the same type of model, now we're just looking at animals supplemented with live Lactobacillus johnsonii versus PBS, what happens at day two. And we were particularly interested in whether there were metabolic changes in these animals. Whether the small molecules produced by an altered gut microbiome could hold the secret to the response to the viral infection. And I don't expect you to read all of this. Here's where we use that mass spectrometry to look at all the small molecules that are produced in these animals in their serum, in their circulation. this is what we see in the control animals two days after we infect them with respiratory syncytial virus. Anything in blue has gone down from baseline, anything in red has gone up. Not a whole lot going on. And I think you'll agree that that's true when I show you what happens in the animals that receive the live lactobacillus johnsonii. Now we see two days after the viral infection in the airways this immense capacity to produce a whole range of amino acids, peptides but in particular lipids and when we saw this list of lipids, we got super excited. Because in this list of lipids are a whole range of things like polyunsaturated fatty acids that we know dial down inflammation. And so that suggested to us that when we alter the gut microbiome of these mice, we change the metabolic output not just of what's in the gut but what's in the circulation of these animals and that that's what leads to the protection against the viral infection in the airway. But we wanted a little bit more evidence for this. So we did one more experiment. We took what we call bone marrow derived dendritic cells. So these are immune cells that are really critical in response to viral infection. And we incubated those immune cells with the blood, the plasma of the animals who received either the control PBS and were subsequently infected or the ones that had the lactobacillus johnsonii introduced into the gut and then were infected. So those ones that had that two-day lipid onslaught that we saw. And then we took those dendritic cells, those immune cells and asked how did they now respond to the virus when they encounter it. Could the products that we see in the circulation change the activity of the immune cells and that's indeed what we found. The immune cells that we know incubated with the plasma from the animals who had the lactobacillus johnsonii now are significantly less inflammatory and they're significantly less activated and they have significantly less lower capacity to present antigen to engage in an inflammatory response. So what this tells us is that by changing the gut microbiome we can change the metabolic output of the system from the gut and we can actually protect the airways of those animals. And it looks like some of this is through the production of these metabolites. What I neglected to tell you is we started looking at some of those metabolites and we did find that one of those polyunsaturated fatty acid conferred this phenotype in the cells. So we were right in thinking that those anti-inflammatory lipids are perhaps the ones that are driving this change in how our immune cells are functioning in this mouse model. So that's all in mice. That's great. But that's a model system. Could the early-life gut microbiome actually be perturbed in babies who go on to develop allergies and asthma. And maybe it's just beyond a perturbation to who's there, could the metabolites being produced by the early life gut microbiome actually be the key to priming the immune cell differentially in children, in babies who go on to be children with asthma. And so we really wanted to ground this in something that was very kind of solid. And so we think of early life microbiome development no differently from how any other ecosystem develops. And we've studied ecosystem development for a couple of hundred years. So they're pretty good framework. We know how ecosystems develop. And one of the things we know about ecosystem development, is that the first colonizers, the first species into a previously pristine ecosystem can actually shape the conditions in that ecosystem and species accumulation trajectories over time. So What this suggested to us is perhaps there's different types of seed microbiomes. Different types of micro biomes in early life that lead to different trajectories of microbiome development. And remember, the microbiome educates the immune response. And we think that that could lead to distinct immune maturation and give rise to health or asthma and allergy development years later in childhood. And again as I mentioned, we began to think about how this might work. And we began to think of what we've seen in the neurology field or the gut microbiome or the cardiology field that gut microbial metabolites can shape remote organ behavior. And we've seen that in our mice so we thought that it's not just about a perturbed gut microbiome in early life it's perhaps the molecules that that got microbiome is producing really skew immune development in those babies. And so one of the first studies that we address this in, was a study of the gut microbiome of healthy babies and high risk for asthma babies. And they're designated high risk for asthma babies because they have at least one parent who has asthma and this is the meconium microbiome. This is the first bowel movement of newborn babies. This forms in utero. And here I'm showing you another one of those plots where it's one of those distance plots. In red, are the high-risk babies, in green are the healthy babies. And you can see they're kind of segregated along this axis. They're spatially separated. They're actually significantly different. So high risk for asthma babies start life with a very different microbiome from healthy babies. And what's exciting and consistent with what ecosystem theory would predict, those babies follow a different trajectory of microbiome development. These are the healthy babies and they accumulate bacterial diversity at a pretty quick clip over the first year of life. In contrast, the high risk for asthma and allergy babies, have delayed diversification of their gut microbiome. And remember, each species of microbe brings with it its own genome and its own repertoire of genes into the gut microbiome. So these babies will have a very functionally distinct gut microbiome. They just don't have the same microbial capacity that a healthy gut microbiome has. But that's simply one study. Can we see this in a population? These are high risk versus healthy controls. This is the extreme. Can we actually spot this just in a population of babies? And so to do this we studied a large birth cohort. Again, this is one of these studies where samples are collected in very early life and the babies are followed out through life and we know whether they, in this case, developed allergy at two years of age or asthma at four years of age. and the part of the study I'm going to tell you about, we had 130 one-month old babies from whom we had fecal samples. So we profiled their microbiota using the the gene-based approach I told you about at the outset, to find out which bacteria and which fungi were present in these microbiomes of these 130 babies. And then this is quite a large amount of data. We became hands-off at this stage. We asked an algorithm can you find significantly distinct gut microbiomes amongst these 130 babies? And the answer was three. The answer always seems to be three. Here again, I'm showing you one of these distance plots. And here you can see that what the algorithm called the three different gut microbiomes, we've labeled them, neonatal gut microbiome one, two and three. Shown in blue, green and red. And again they're spatially segregated. They're significantly different in their composition and actually calling them neonatal gut microbiome one, two and three. Those classifications explain about 9% of the variants in microbiota as we see in these 130 babies. But the key question is does starting life at one month of age with one of these gut microbiomes relate to the clinical outcomes we see at age two and age four. And the answer was a resounding yes. Babies with the one-month old NGM3 gut microbiome were at significantly higher risk of developing atopial allergies at age two and asthma years later at age four about three times more likely to develop these diseases. What was different about these gut microbiomes? Well, we found was it wasn't just a loss of bacteria that we saw on the high-risk NGM3 baby gut microbiome. We also saw that they were highly increased for, what we consider to be allergenic fungi, rodatorola and Candida. So this isn't just about a loss of bacteria, it's also about an increase in fungi in the gut microbiome of these babies. And using mass spectrometry, we asked is the metabolic output of this gut microbiome distinct? And we found that yes it is and I'm not showing you another one of those crazy plots where you can't read anything but I'm gonna summarize and tell you, just like we saw in our mice, the babies who went on to develop allergies and asthma had significantly reduced polyunsaturated fatty acids amongst many other lipids. And they also were highly increased for this one lipid, 12,13 DiHOME, a diet oxyfatty acid. So what all of this pulled together suggests to us is that the NGM one and two microbiomes are actually tolerogenic. They might be educating the immune response in a very different way from the NGM3 microbiome in the gut which is full of potential pathogens and is metabolically very much altered. But how do we test this? We need to really think outside the box. All we had was stool from these babies. Nothing else. And so what we thought is we could take immune cells from healthy adult donors and we specifically took the immune cells that govern allergic response, dendritic cell which present antigen to T-cells and educate the T-cells and dictate what they will be when they mature. And so we purified these specific populations of cells, remember, from healthy adult donors, and we co incubated the dendritic cells with the cell free products of the gut microbiome of the high-risk NGM3 and the low risk NGM1 babies. So that we could prime those dendritic cells. We let them sit for a while and then we cultured them with the naive T-cells and we were particularly interested in what we would see with TH2 cells, remember the ones that produce inflammatory cytokines, and T-reg cells, the ones that dial down inflammation. And what we found was that the cells that were co incubated with the NGM3 fecal water from that one month-old gut microbiome had far greater numbers of TH2, allergic T-cells, they produced more IL-4 and those T-cells were significantly less likely to be regulatory T-cells. So remember I told you the cardinal immune features of allergy and asthma at the outset of the talk, here we can recapitulate them using the fecal products, the gut microbiome products of a high-risk one-month-old gut microbiome. This is years before we ever diagnosed the disease. But we were really interested in asking what are the products in that kind of fecal milieu that produce this immune dysfunction. And we focused initially on this lipid that I told you about 12,13 DiHOME. Because it kept coming up in all of our analyses. No matter what way we carved out the data, we kept coming back to this molecule. And so we asked whether this molecule could recapitulate features of that immune dysfunction I just showed you that we produce with the fecal water. And what we found was that critically this one molecule, as you increase the concentration of it, you reduced those regulatory T-cells and you reduce their capacity to produce the anti-inflammatory molecule IL-10. So now we have a molecule that looks like it actually skews a very critical part of the immune response that we need to dial down allergic inflammation. So we wanted to test that in a mouse model. What we did is the same mouse model as I introduced you to earlier on, but here three hours before we challenged the airways with cockroach, we injected this one lipid into the gut of a group of these mice and asked whether it exacerbated the allergic response in the airways of these animals. And what we found was a resounding yes. Here are our controlled animals. Nice, clean air spaces, here the sensitized animals. All these little black spots are inflammatory cells around the airspace. As you can see they're constricted, there's pink mucin there. These are the animals that got that one lipid into their guts before we sensitized them. Now we've absolutely occluded their air spaces with mucin and inflammatory cells. Ad consistent with what we've seen in a test tube, these animals have significantly reduced regulatory T-cells in their airways and they have significantly increased IgE, that antibody that we know is associated with allergy and asthma in their circulation. So just by the simple introduction of this one lipid into these mice, we can exacerbate their allergic inflammation in their airways. And it suggests to us that elevated concentrations of this lipid in the very early life gut microbiome could actually have the same effect on that critical population of immune cells in these babies, reducing their capacity to dial down allergic inflammation. But we wanted to dig a little bit deeper. This molecule is the product of metabolism of linoleic acid. Linoleic acid is plentiful in breast milk, it's plentiful in formula. It's a key lipid in very early life nutrition. What we found in the healthy babies is that their fecal microbiomes are highly enriched for this other metabolite DiHOMEgamalinoleic which is a precursor to a whole range of anti-inflammatory products. The high-risk babies we had shown, were highly enriched for this lipid. So what we hypothesized is it's actually the gut microbiome of these babies has the capacity to make 12,13 DiHOME from linoleic acid. And we know that the final step to make this product is catalyzed by an epoxy hydrolase, a special type of enzyme that converts 12,13 EpHOME to 12,13 DiHOME. So we went kind of dumpster diving in the gut microbiome. We went looking for microbial epoxide hydrolase genes. And we simply quantified them in the gut microbiome babies who went on to be healthy or those who went on to be ectopic or asthmatic years later in childhood. And remember this is the one-month old dot microbiome. And we found that the babies went on to develop disease were significantly enriched for bacterial genes to make this lipid. Not only that, they also had far more of that lipid in their feces. And we went on to functionally test these bacterial genes and found that three of them could specifically make 12,13 DiHOME, this lipid that seems to be so critical in promoting allergic inflammation as we've seen in our studies. And these are species that every baby has. They have them in their meconium microbiome. Every baby has an Enterococcus faecalis, every baby has a befitted bacterium bifidam. But we think the difference between health and disease, is that the babies who have these species with these bacterial genes are the ones that go on to develop allergies and asthma. And we show this is true using two birth cohorts. So we showed that for every doubling of the number of epoxide hydrolase genes in the one-month-old gut microbiome, there's a significant increased risk of developing allergies and asthma years later in childhood. And that's also true for every nanogram increase of that lipid 12,13 DiHOME in the feces of these babies. And that's consistent when we look at a completely different cohort of babies based here at San Francisco at UCSF. So what this tells us is we've gone from a gut microbiome perturbation to identifying what we're thinking of microbial risk genes. These genes confer increased risk of developing allergies and asthma years later in childhood. And because of these genes and their products we're beginning to understand why these babies develop disease. These microbial products really skew immune function and reduce the key immune cells necessary to dial down allergic inflammation. So we've got a new model for a pathway by which allergy and asthma may develop. It's one in which babies inherit microbes from their mothers and they begin to develop their gut microbiome. And those have a specific type of gut microbiome that is enriched for microbial capacity to produce this lipid 12,13 DiHOME, they have reduced T-regs, these key immune cells to dial down inflammation. We know from our mouse studies that this lipid escapes the gut and actually enters the circulation and goes to the airways. And we think it exerts the same effect there, reducing these key immune cells in the airways. And what that gives rise to is a lack of capacity to respond to pathogenic microbes we encounter with every breath. And those babies build up a pathogenic airway microbiome over time and that's what gives rise to the diagnosis of asthma in these children later in life. We know that this starter distinct perturbed gut microbiome gives rise to a different trajectory of microbiome development in the gut of these babies. So what can we do? Well, we've rationally designed a synthetic cocktail of microbes to be introduced in very early life, day one, day of delivery, to babies at high risk of asthma. These microbes encode all of the functions that these babies are missing in their starter microbiome. And the idea is that these microbes shape the immune milieu around them and that that governs the trajectory of microbiome development and will allow for appropriate microbiome development in early life and also will change the metabolic output. We will re-engineer the microbiome in these babies to change the metabolic output, change the interaction with the immune response and prevent asthma and this product is currently in clinical safety trials first before we use it as a treatment but it's not just about allergy and asthma. We also are performing studies on the very early life gut microbiome and obesity. Another plague on our nation. And we're finding very exciting and somewhat familiar findings. Here again, we find three distinct gut microbiomes in a much larger cohort of babies. Over 400. One of them confers a significantly higher risk of developing overweight and obesity phenotypes in childhood. Those babies are more likely to be formula-fed. And what we found is that the products of that gut microbiome change how the cells lining the gut take up and release lipids. In fact it accelerates that process and so that we think that that excess lipid is entering the circulation and if it's not used up it's laid down as adipose and this could be a mechanism by which these children ultimately develop obesity and overweight phenotypes later in childhood. Also offering the opportunity that perhaps again, early intervention in these high-risk babies could change the course of their microbiome development and metabolic output of those communities and change their course of health. And again, it's not just obesity. Tiffany Scharschmidt who's an incredible faculty member here at UCSF is showing that this happens on the skin as well. The first microbes that colonize the hair follicle change or influence the immune milieu in that hair follicle and dictate which other organisms get to come to the party and co-colonize in that niche. And this is offering opportunities for again, changing the microbial host interaction to change the course of disease development. We've also been looking at this in terms of the upper airway microbiome development and again have shown that babies with different trajectories of microbiome development in the upper airways are at higher risk of asthma and there's specific colonization patterns that we've identified in the upper airways that not only increase the risk of asthma, they also increase the risk of the exacerbation in those children. So again, thinking very differently about this, thinking about early life as an opportunity to re-engineer the microbiome in a manner that changes the physiology of the host and alters the trajectory of disease development in these individuals. So what have we learned from this lecture? We know that very early life is a critical period in which we build our microbiomes. Not just in the gut also in the airway and at other sites across the body. And that the types and more importantly the genetic capacity of those microbial communities is really critical to promotion of health in humans. We know that there's distinct founder-populations of gut microbes in very early life that strongly shape immune function and that relate to childhood disease outcomes. So we believe again, we've got this canary in the coalmine, we've got this very early perturbation that gives rise to a downstream disease development years later in childhood. And part of that is that the microbes that are there are producing specific small molecules that are skewing immune function. And we believe that this is occurring in the earliest stages of postnatal life and then that skewed immune function, that inflammatory milieu in the gut, is really strongly selecting the types of microbes that are permitted to occupy the niche in the gut and that's why we see a lower diversification of those gut microbiomes over time in these babies. And we're really excited because we really believe that this is a new field that is changing the face of human biology and we are delighted to just this year, launched the Benioff Center for microbiome medicine here at UCSF. We're excited for what this field can do and I've just really shown you a snippet of the background and some of the exciting work that's going on in the field. Within the center, we're leveraging for example, healthy periodontal microbiome to find new microbes and molecules to tackle periodontal disease. We're looking at how the gut microbiome relates to multiple sclerosis. Sergio Bernzini and neurology has really strong data linking this disease with the gut microbiome and he's now actually engaged in a fecal microbial transplant study of this population asking whether that can improve symptomology in his patients. Katey Pollard who's here at UCSF is a computational whiz and she's the one that that's allowing us to look past who's there and look at specific genes that are the differentiator between health and disease development in our microbiomes and in our patient populations. And then finally we're delving deeper into our trials of fecal microbial transplant to understand how does it work, which microbes matter and which molecules matter so we can build bespoke synthetic microbial communities that are tailored to specific patient subsets and not just necessarily go in with the blunderbuss fecal microbial transplant approach. And we believe with this we can actually enhance efficacy in this population. There's other things we're doing. We're leveraging microbes to combat microbes. Because that's what microbes do naturally in their ecosystems. they antagonize one another and we're leveraging this knowledge. We're using phagers Phagers like viruses that bacteria have and they are very specific in what they target and we're asking whether we could use phage therapy instead of antimicrobial therapy. Can we be really specific and go after key pathogenic organisms that we believe are driving the pathology in our patients. In our upper airway studies for example, we've got a couple of very key target organisms, Moraxella catarrhalis. we've seen a crop up across multiple different studies and we're now gonna target it with phage therapy to ask whether we can specifically take out that organism and re-engineer the microbiome of individuals that have these colonization patterns associated with their disease. There are efforts, not necessarily at UCSF, but at other sites to leverage microbes to express specific cargo in the gut to produce the IL-10 molecule, for example, that dials down inflammation. We're working very hard at UCSF to understand diet and the microbiome. I showed you a snippet of work from the Turnbull lab. We're using diet in a pilot study in ulcerative colitis patients to ask whether we can change the microbiome of those patients and induce remission by diet. We're also as I mentioned, developing bespoke synthetic microbial cocktails and ultimately I believe that is the combination of diet and microbiome or specific substrates and microbiome symbiotics that I think will be most efficacious in our patient populations. And ultimately our goal at the center is to focus on the early life microbiome as an opportunity to intervene early to prevent disease and to develop novel therapeutics to treat the variety of diseases that our patients suffer from. And with that I am very happy to take any questions. (applause) - Yeah, the question is about probiotics in food and probiotics themselves over-the-counter products. It's not an FDA regulated area. Although they have been trying to really hone in on claims being made by companies about what probiotic supplements can actually do. I'll also say that not all probiotics are equal. There are differences in A, the types of microbes that are in probiotic supplements and in B, the quantities of microbes, of viable live organisms in those products. And that vary very tremendously across products on the market. I think what's really key is two papers that came out last year that I think were really critical in our understanding of how probiotics may work and these were studies looking at the gut microbiome of healthy volunteers who consumed a probiotic product. And what they showed was whether this species in the probiotic were basically allowed to engraft or were capable of engrafting in the gut was entirely dependent on the microbes that were there already. And again, this gets at this idea that the microbes, the first-come-first-served. The microbes that are there already dictate who gets to come into the party and that was shown very clearly. And that may explain why individuals may respond very differently to microbial introduction. Be it by probiotics, be it via microbes that are on the food we consume. Our microbial encounters and which microbes get to engraft anywhere in our system seem to be strongly influenced by the pre-existing microbiome that is there already. So I think we can do better. I think there's some nice proof of principle out there and in fact some products have shown efficacy in controlled clinical trials but I think there's a broad variety of products out there. They're really not equal. And in fact there's been some studies that have shown that in some cases some of the products, A, don't contain the species that they're supposed to contain and actually contain a different species that could be detrimental to the consumer. So the question is you know how do you explain meconium microbiome? Does it come from the mother, where does it come from. And if you're gonna treat, why treat at birth and why not treat the mother. So a few things: meconium is swallowed amniotic fluid. It is by definition formed in utero. In a study I didn't show you that we are preparing for publication is one in which we've actually asked when are microbial encounters occur in the human fetal intestine. There's a lot of controversy around whether there's a microbiome associated with the placenta. The kind of jury's out on that. But we actually asked what's happening in the intestine of the fetus. Because there we know through previous studies, not from our group but by other groups, that the immune system has already started to evolve and develop. And by 13 weeks gestation in humans, has the capacity to sense and respond to microbes. So we looked at mid gestation and found that there was a very sparse microbial signal in human fetal meconium but that we could find microbes there. They're in these tiny little pockets, they're kind of tightly densely packed together. They're embedded in the mucin so this is not contamination and they're in a subset of the samples we examined. We found an organism whose presence was correlated with a specific type of immune cell response. We weren't able to isolate that organism from the fetal meconium using media that traditionally selects for that type of organism. We had to add pregnancy hormones and an immune cell population into the selection media to be able to isolate that organism. We've sequenced its genome. It looks like other organisms that are phylogeneticly related but it has unique genomic features that we've not seen in other species, even those that are highly related. Suggesting that it may be highly evolved to be in fetal intestine in utero. We think that that process probably ramps up later in pregnancy because the this communities that we detect in and postnatal meconium, the first bowel movement after birth, they're simple but they're more complex than the really really simple communities that we saw in the fetal intestine. Why not treat the mother? We don't know enough. It's what I would say. Our studies have shown us that, other studies have shown that there's a difference in the three-month-old got microbiome related to allergy and asthma, our studies have shown that through at one month of age and in meconium and that's what's driven us into the fetal intestine to ask whether microbes are there but we know virtually nothing about the maternal microbiome during pregnancy. There's a sparsity of papers out there. We know it changes with advancing pregnancy. We don't know why that happens. We don't know what the implications of that are on downstream health outcomes of the babies. And I guess the reason for intervening at early postnatal life is that's the inflection point in microbial development. That's when these communities are at their simplest and when we believe there is greatest real estate open in the gut for colonization. And rather than we will perhaps ultimately intervene in pregnancy but until we know a lot more in that field, that's not something that we are comfortable doing. We do know and we have lots of different studies telling us what high risk for asthma babies are missing in terms of microbial capacity from the get-go, from the day they arrive out through the first year of life. And for me that's a safer approach to take rather than playing with what's happening in utero when we have no idea the implications of what we may do. Yeah I mean I have to say I would preface the overuse of antimicrobials and its effect on the microbiome. I think there's a number of things that have gotten us to this place where we've extinguished a number of microbes that we think are probably critical for human function and health. One of them is plausibly antimicrobial use but there's many other things. Diet for example has dramatically changed. We know that antimicrobial administration causes an acute and sometimes pervasive drop in the diversity of microbes in the gut but your response to antimicrobial treatment again is predicated on which microbes you have in your microbiome. Antimicrobials have saved lives. We have to first and foremost remember what we've used them for but in doing so we may have created a bigger issue with chronic inflammatory diseases is the thinking. But I will say that I still think they have great utility. In our fecal microbial transplant studies with ulcerative colitis patients when we simply did a single colonoscopic delivery of the fecal microbial transplant, no one responded to the treatment. When we pre-treated the patients with antimicrobials and then gave the colonoscopic delivery followed by a month of treatment, that's when we got to 40% efficacy. So I guess it proves principle that it clears the decks for colonization and there is utility. And I think there's been a lot of effort for improved antimicrobial stewardship. I know I've gone recently with my child who had an earache and we were given a prescription but told to wait 24 hours and we never filled the prescription. And I think that there's a lot more awareness. We didn't know about this field 15 years ago. We didn't know the impact or the, we really thought about antimicrobials in terms of antimicrobial resistance. We didn't consider what we are doing to the microbiome with their administration. So I think if anything been beneficial and prompting greater antimicrobial stewardship across the health based system. There's one great paper out of Israel a couple of years ago where they studied just that. They studied Aspartame which is an artificial sweetener and they showed that A, it impacts the microbiome and B, that the glucose spikes that they found in patients, participants who consumed the artificial sweetener, were actually higher than that of a glucose hit. So it it yeah, yes, yes and yes. It affects the microbiome and it is really changing the kind of metabolism of the system which we believe is really what's driving the physiology of cells in the human super organism. So limited information on it but what has been out there has been pretty interesting. They may not be doing what we think they're doing. So just to be, the question is we've talked about introduction of fecal material in children. I haven't, I'm talking about introduction of very specific microbes into babies not feces. What about adults? Great great question. Yeah, I mean we believe that you can manipulate and re-engineer the microbiome. I think it's a higher bar in established chronic disease and I think we're beginning to understand why. We're starting to look at whether these microbial molecules actually don't just change what the cells of the host are producing but also maybe hardwire the genome of those cells and we've evidence that that actually occurs. So you're really undoing several layers of selective pressure on the microbiome from the host side. So I think that that's why you require a month of treatment in the case of autism spectrum disorder children to see a significant reduction in symptomology in those children. And I would argue that perhaps for those with chronic inflammatory diseases, it may be even more long term treatment to manage their disease symptomology. In some severe cases, the jury's out whether we can ultimately bring back that system to one of a healthy system but we'll certainly try. So the question is whether there are studies that have examined the microbiome in adults with obesity. There's a large body of literature on that and I would say that there are some of the seminal studies in the microbiome field. The very earliest studies showed that the obese gut microbiome is significantly different from that of the lean microbiome. And even in the simplest terms, just the relative ratios of the key groups of microbes in the gut are kind of firmicutes and Bacteroides or a ratio of three is to one in lean individuals and it's more like 30 to one in obese individuals. And that's what prompted those studies asking whether you could transfer an obese phenotype by just simply transferring the gut microbiome to those germ-free mice. Whether there are approaches to manipulate the gut microbiome to try and undo that, in one of those early studies they did show that an intervention that comprised of calorie controlled diet and exercise regime led to weight loss and to the return of the gut microbiome back to that 3:1 ratio compared to the obese microbiome. It was a year of intervention. And this is the thing, thinking about what it takes to get to those and the severity of those chronic conditions I think it's going to be a long-term intervention to really bring that system back towards something that resembles a healthy microbiome. The question being about H. pylori being a carcinogen. I think what's really important to think about here is how these organisms behave is entirely related to their microbial peers and their local ecosystem conditions. And thinking about Helicobacter as a single thing to target, I'm I'm not sure that that's the right way to go. Marty blazer would counter that loss of Helicobacter Pylori is associated with increased allergy and asthma development and western worlds. So I think we have to think a little bit more critically about what these organisms are doing, how they're functioning and really targeting the function rather than the organism. Because, most of us have Helicalbacter Pylori but it's controlled in healthy conditions both by the conditions in the stomach and by the organisms around that Helicobacter. So I think as we dig deeper into understanding specific mechanisms by which specific microbes drive disease processes, we become more precise in how we target those disease processes via microbes. Okay, thank you so much. (applause) (upbeat music)
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Channel: University of California Television (UCTV)
Views: 182,045
Rating: 4.8617282 out of 5
Keywords: Gut Microbiome, health, flora, food, nutrition, intestine, stomach, disease, immune system
Id: XCaTQzjX2rQ
Channel Id: undefined
Length: 82min 27sec (4947 seconds)
Published: Mon Dec 23 2019
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