Microbiome Insights is proud to be the sponsor of season 2 of Ruairi Robertson's Biomes Podcast.
In this episode Ruairi talks with Dr. Marie-Claire Arrieta, a professor at the University of Calgary. You'll find topics discussed such as:
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Ruairi Robertson:
Hello, and welcome back to Biomes episode five of this second season, sponsored by Microbiome Insights. Now, when you hear the phrase gut microbiome, or even just microbes, you most often think about bacteria, don't you? However, a huge proportion of your intestinal microbes are other types of microorganisms like viruses, archaea and fungi. These other microbes, however, have been studied in much less detail than bacteria. And we know less about what they're doing to your body. And this is fascinating if you think about it as there are many more viruses, for example, in your body than there are bacteria, but we just know much less about them. In this episode, I speak with Dr. Marie-Claire Arrieta of the University of Calgary. Dr. Arrieta is an expert in intestinal fungi, especially in younger children.
Ruairi Robertson:
We know that in infant, gut bacteria is important for the development of their immune system. But her research has shown how important different types of fungi are. She has shown that these gut fungi may help prevent children developing asthma in later childhood. We discussed this research about these neglected gut microbes, myths and realities of the notorious candida species in the gut, and the exciting future of microbiome research beyond bacteria. This season of Biomes is sponsored by leading microbiome services provider, Microbiome Insights. Microbiome Insights provide end to end microbiome sequencing and bioinformatics services, including assessment of the fungal microbiome using ITS2 sequencing. Find out more at microbiomeinsights.com and mention this podcast to get your free study consultation.
Ruairi Robertson:
Well, Claire, thank you very, very much for agreeing to have a chat. It's great to chat you all the way from Calgary and learn about what you're doing and with the fungal microbiome. So, how about we just start off and let me know a little bit about your background in microbiology and microbiomes. From what I read, you were kind of originally involved in kind of clinical microbiology and then looked at IBD, and now you're kind of very much involved in infant microbiomes. So, where did you start and how did you get to where you are now?
Claire Arrieta:
That's right. So, my initial background is in clinical microbiology. For grad studies, I was involved in gastroenterology signs. So, understanding the physiology and the immunology of the GI tract and how important it is for health, not just in the gut, but also in other parts of the body. So, I finished my PhD in around 2010 and this was around the time where those first large microbiome studies were coming out. And here, we were trying to study the gut and all the ins and outs of it and how it functions, what it does. But for the longest time, I think that GI research was not really paying attention to this very large amount of microbes that normally resides there permanently. And from my microbiology background, I became really interested in trying to study that crosstalk because of how the gut functions and how this massive amount of microbes contribute or not, to its functioning.
Claire Arrieta:
So, I decided that I wanted to do a post-doc going back to microbiology and to try and study that the microbiome and understanding that, at least until now. In order to study it, we needed to apply a sequencing and bioinformatics methods. And then I didn't have any training on that. I was mainly a classic molecular biologist and microbiologist up until then. So, I moved to Vancouver and this is when I became part of the Finley Group. And he was at the time, one of the few people that was looking at this. And in collaboration with other microbial ecologists at UBC, we started studying the gut microbiome of babies. And then I became fascinated by it. Now, I was able to really mix my knowledge in GI biology with what we're learning, this very new science of the microbiome.
Claire Arrieta:
As more studies started to happen at that time, coming to the conclusion that that early in life is a very important period for both GI functioning in general body development, but also in terms of the ecology of the microbiome. We're born without one and we start to gain microbes as we age very, very rapidly. And there's a lot of ecological shifts that happen early in life of which we still know very, very little. And our body in many of our systems rely on that initial colonization to finish its training, if you may, or its development. So I knew that there was going to be years and, I guess, careers worth of knowledge there and decided to stay and in that field.
Ruairi Robertson:
Great. So you were really at the beginning of all of this. You were kind of have been there from the start almost and watch the field grow.
Claire Arrieta:
Yeah. Although, I think that truly microbiome science start up before it merged into the clinical science of things, right? And there's pioneers that were merely interested in studying microbial ecology used in the environment. Those are the really pioneers. And those started a bit earlier than that, maybe 10 years, a bit more 10, 15 years earlier. But yes, when it started becoming more integrated into medical science, I became part of that, yes.
Ruairi Robertson:
Great. Well, whether it was at the start or not, I think you've kind of carved your own niche anyway, in the field. And because for years now, since we've appreciated the complexity of the microbiome and its diversity, most of the focus has been on the bacterial component. All of these numbers are thrown around that we have over 1,000 bacterial species in the human gut, where 99% bacterial genes, whichever way you count these things. But really, there's a lot of unknown microbial matter living inside us as well. And one of that is definitely all the fungi, that live inside of us. And little less is known about that, but a lot of your work has focused on that in recent years. So, what can you tell us, kind of to start off, very basically about the fungal microbiome and the gut? What relative contribution does it make to the gut in terms of how much is in there? What are the main species? And do they remain stable over time?
Claire Arrieta:
Well, in general, fungi are extremely successful forms of microbial life, right? There in every terrestrial and aquatic environment that they've been looked out. And as with any other ecosystem, the gut also has fungi. So there's nothing surprising there, I think, as you say. What was surprising is that until now, probably because microbiome was such a new science, at least human gut microbiome, people were paying more attention to bacteria and rightly so, there's just too many of them there. But with any ecosystem fungi as well as other forms of microbial life, are a part of this ecosystem. The interesting part about fungi, and this comes from the field of infection biology, so that mycologists that have studied fungi for years now is that we know that they have other mechanisms of potentially gaining access to the host, and that our immune system and other systems have specific different distinct mechanisms to recognize them and to identify them and then to react.
Claire Arrieta:
So the way we react to a fungal infection is not the same way that we react to a viral infection or a bacterial infection. In some ways it's similar, in some ways it's not. And another part that got me really interested, and this was at the time that I was having babies myself, my kids are a bit bigger now, is that yeast infections in babies are more common than in older people. And I became just really interested in trying to study that. So, what happens early versus later, and what happens to fungi during our lifespan. And rightly so, when we started studying them in a couple of course studies, and now when we study them in mouse studies as well, we have found that fungi are pretty adept at forming part of the gut. But that initial colonization phase, it's a pretty unstable phase.
Claire Arrieta:
That ecosystem hasn't really established. And there's a lot that can happen that can change the state of that ecosystem until it reaches a more balanced state or more stable state. And one of those factors that can do this is the presence or absence of fungi. So, that's one of them. Another one is how fungi can respond to perturbances to that ecosystem in the form of an infection or in the form of, for example, an antibiotic. So, one of the things that we're studying and that we're learning now is that, fungi just like bacteria respond actually quite strongly to things that may happen early in life. And by doing so, they may cause a result or they may lead to a different immunological response. Now, in parallel to this, one of the things that we know now is that early in life, there's this critical period of time during which the immune system, not just the immune system, but we're speaking about the immune system now, but the immune system is very responsive to signals.
Claire Arrieta:
It's almost eager to learn. It's very permissive also of changes. So, those alterations that may happen in the ecology of the microbiome may have a stronger or a more longer lasting consequence if they happen at that moment than if they were to happen later in life. And what we're finding now is that fungi are part of this group of signals that can result in these immune education or miss-education events. So, we're now in the midst of that, on the beginning. I started my group about four years ago, but learning a lot because not that many people are studying fungi. Although it's changing.
Ruairi Robertson:
There's more of it.
Claire Arrieta:
I see slightly more studies coming out, but it's really neat because it's very new. So, there's a lot of potential of discovery.
Ruairi Robertson:
Right. So it's similar, we know a lot about bacteria that are acquired in our early periods of life, which you're studying. And how does that work with fungi? What are the first fungal colonizers of the gut? Are they coming from the mother as well? Is it the mother's gut? Is it mother's vaginal fungal species? Have those studies been done to track where the fungi are coming from and what exactly they are at the very start of life?
Claire Arrieta:
So, tracking studies in order to really understand where bacteria are coming from, they require a pretty high resolution sequencing or genetic based studies, right? Because you shouldn't just follow the species, but you really have to follow strains. And those have definitely be done for bacteria. They have not been done for fungi. Now, there have been studies at the species level that have compared the type of a fungi that we have in stool versus where else do we find them? What we find in fungi is that yes, just like bacteria, we have different fungi in our skin and different fungi, in the case for women, in our vagina as well. But one of the different things, if we compare that to bacteria, is that we have more fungal species able to inhabit different parts of our body.
Claire Arrieta:
They can be less specific. And what's really interesting is that many of them are free living fungi too. So, they live in the environment, they can be fine in all sorts of places. And that actually mimics what has been described in other environmental ecosystems as well. So, where are they coming from? We exactly don't know. But based on the species similarity, we speculate that they're definitely being caught up from the vaginal canal because there's a lot of candida species there, and those have been described in that body side for a long time. There's also skin organisms. So, one of the ones that we're studying quite a bit, it's quite interesting microorganism, is this yeast known as malassezia. It's been found in skin as well as the environment. But it has been fine in skin for a while, and now we're finding it in the gut as well.
Claire Arrieta:
Now, another important difference that we're still in the process of trying to make is which fungi are truly gut dwellers and which ones are just transient? Which ones are we just finding because we're measuring stool. So, with mice, we're able to ask those questions. And we find that, at these we focus on the mice, there's cases for both, right? There's some that we can continue culturing from the stool and that we can find actually living in the gut mucosa. But some of them, they just passage through the gut and this passage appears to be short lived. We're not there yet to fully understand this in humans, we would speculate that there's some very abundant yeasts like candida species or even malassezia species that are truly dwellers of the gut. Whereas there's some other ones that, because fungi are everywhere in the environment, is also easier to find their genetic material in the gut as well.
Ruairi Robertson:
That's really interesting because you don't tend to see that as commonly for bacteria. Bacteria seem to be more niche specific, I suppose, that there's bacteria that have evolved and I can only really survive in conditions like the guts. I mean, I'm not talking about every species in the gut, but quite a number of them. Whereas you're saying that fungi seemed to be able to adapt. Is that because they are more complex organisms that they're able to have these genes or whatever it is to be able to survive in, let's say, in beer or in bread and also in the gut or in soil
Claire Arrieta:
Absolutely. Absolutely. There are a lot more prolific, they have bigger genomes, they have a more sophisticated machinery to use different types of nutrients and survive in different environments. There's a lot of fungal species that we're finding that yes, they can survive in anaerobic conditions not as well, but they will do so for a long, long period of time. Whereas for bacteria, some of them, especially some of the ones that have been described in our guts, there are strict anaerobes, right? And that have mechanisms of survival in the environment, right? But what we're finding with fungi is that yeah, you kind of tend to find them everywhere. And because of that, you have to be a lot more careful in not assuming that they're living there and that they're a part of that ecosystem from a permanent point of view.
Ruairi Robertson:
Right. And do you have any idea how our fungal microbiomes have changed over time? We know a lot of these interesting studies showing us how our microbiomes, our bacterial parts of our microbiomes, anyway, are becoming less diverse. If we look at these hunter-gatherer tribes and look at their bacteria and microbiome, they're way more diverse. They have all these species that we seem to have lost. And there's also these other really complex worms and other kinds of more complex organisms which people in kind of very rural settings like that tend to contain in their gut and we don't tend to contain them in the Western world. So, what do we know about that with fungi? Have we lost fungi in our gut? Are we acquiring different ones with westernization or how has that changed historically as we, I suppose, industrialize more?
Claire Arrieta:
Yes. It seems that that's the case. Although there's very few studies. We've been involved in one of them, but yes. So different fungi that have been found in babies in South America compared to Canadian babies, and less fungal sequences that have been found in that Canadian baby. You find them, so they're there. It's not that they're completely missing. But yes, I would speculate that there has been a reduction and also a shift in the type of fungi that we acquire. Of course, when one compares two different places that are different in socioeconomic conditions or in industrialization sort of parameters, one also has to take into account that there are also different geographies, right? So, one of the things that will really change that type of life, including microbial life that you find in a place, in this case was in Ecuador, and it was in a tropical spot, very humid spot of Ecuador so you would expect more fungi.
Claire Arrieta:
Because the place is a lot more humid than if you look at Canadian babies. But yes, there's definitely changes when we looked at different human populations. How they happen, we're still not sure. One of the things though, that I think supports this notion that as we have cleaned up ourselves and our societies, we have lost some of our microbial companions, if you may, is that the studies of mice that have been re-wilded into the environment. So, of course, we all use laboratory mice and these come from strains that have been passaged for many, many years, and they have been raised and born for many generations inside of laboratory spaces. And there's been really interesting work where they have released these animals into just outside the environment.
Claire Arrieta:
There's also been experiments where they have tried to colonize germ-free mice with microbiomes from wild rodents as well. And in those cases, what you find is that, yes, the diversity is a lot higher outside than compared to the classic laboratory mice. And one of the features is the appearance of a yeast. So, in very clean laboratory mice, not in all of them, but one of the things that we have found is that it's very rare to find fungi. In fact, we almost have to give it back to them. But here we have the stories showing that you just let them outside, not only do they acquire yeasts as well as other eukaryotic forms that you were alluding to before, but then there's the big immunological response that happens from that.
Ruairi Robertson:
Right. And so, what kind of proportion do fungi makeup in the micro-biome? Both in terms of, I suppose, just their physical amount, but also I suppose, in their genetic potential. So, the proportion of them being there, but also the proportion of how much they're contributing, I suppose, to microbiomes? Do we have kind of estimates of that?
Claire Arrieta:
Well, there are some estimates about 0.1% if we look at just the accounts of cells or colony forming units, as we would use in microbiology. They have much larger genomes, about 100 to 200 times the size. At the same time, one of the things that I've come to learn, and this is from the field of community ecology, is that when you look at ecosystems that have, of course, different forms of life, they form all these structures or webs. And in many cases, these webs are going to be established from a number of different drivers. But one of the most important ones are food webs or these trophic levels of who eats who, and who eats what other ones are making. And those are really one of the stronger forces of ecosystems.
Claire Arrieta:
And what we have found is that in microbial ecosystems, just like in macro ecosystems, you don't really have to be numerous to have a very impactful role in that web and in that food web. And the classic example is the predators. If you look at ecosystems out in just a microbial world, right? You don't need that many wolves or you don't need that many lions to have a massive effect that in many different species in an ecosystem and even more importantly, in the production or the productivity of these ecosystems, so the functionals component of an ecosystem. What they have studied in microbial ecosystems is very similar. The presence of protists, for example, these are animals that actually feed on bacteria as their main nutrient source, can be very large. Even though you can compare the number of protists to the number of bacteria that you have, or the number of viral particles that you have.
Claire Arrieta:
And the same can occur with fungi, especially because they have this really unique, if you may, ability of changing their biochemical machinery to use different types of nutrients that can be present or not in the gut. So, yes, numbers are important and genome sizes are definitely even more important. But what I've come to learn is that numbers are definitely not everything. And that in fact, having a smaller numbers of important member of an ecosystem may be an advantage versus having many numbers.
Ruairi Robertson:
Right. Yeah. I like that analogy. So, that fungi and the gut could be kind of like the wolves or the tigers. They're central to that web or that hierarchal chain of feeding, I suppose, around viruses or bacteria or whatever.
Claire Arrieta:
Yes. Yeah. And from a predatory perspective, not so much fungi, because there's a few that will digest bacteria, but for the most part, they're really good at just eating what many different fungi are producing so they can compete for nutrient sources in a more effective way. But another thing that fungi are really well known for, and again, you don't need to have many fungi for this, is antibiotic production. So, they have many mechanisms of interacting with a bacterial world, if you may, that can give them an upper hand, or the opposite of that in this micro ecosystem.
Ruairi Robertson:
Right. So it sounds like from what we know, their main functions are to control that ecosystem and what's in it. Produce antibiotics that may be control certain types of organisms that are in there. Do they have any other kind of main functions like what has been characterized for bacteria, that maybe they produce vitamins, do they digest certain nutrients? Well, you've mentioned kind of immune interactions. Is there anything else, kind of these clear functions, that some of these fungal species have that we know about?
Claire Arrieta:
Not yet. So, this is very much at the edge of what we're trying to find out. We do think now from some early experiments that they have a role in modulating our energy metabolism. Comparing mice that have fungi with mice that don't and looking at as several metabolic markers in the host, we find differences. But it's still very early to understand how that is occurring. But I actually speculate that the more we look the more we'll find.
Ruairi Robertson:
Right. Well, I mean, previously in the past, people have looked at fungi as they did bacteria, I suppose, in their kind of pathogenic state and how they cause disease. And so, I suppose they can, depending on the situation, depending on the environment, they can be what some people call as, patabiomes, so that they're perfectly normal and they're present in healthy people, but in certain states they can become disease causing. One of my favorite actually examples of this is a really rare condition called auto-brewery syndrome where some people have some fungi in their intestines and actually produces alcohol and makes them feel drunk. Very, very rare, but in certain states, fungi can cause disease. And that's what we know a lot about them. So, a lot of people, especially in the fields of nutrition interested in microbiome, become really interested in candida, and say that, "Oh, I think I have a candida infection." Whereas we all have various strains of candida, but it's just in certain circumstances they can become disease causing. So, have you looked into this? Or what do we know about candida, about its normal functions and why it can become disease causing in certain circumstances?
Claire Arrieta:
What we have found is that candida, as well as other yeast, has the ability to flare or overgrow, but only, and this is a feature of these opportunistic pathogens, only when given the advantage to do so. So, on its own, it's kept in check by many other, mainly, microbiome driven mechanisms. So, bacteria produce a ton, a ton more in general, biochemicals in the gut, many of which have antifungal properties, short-chain fatty acids is one of them. So, if you have a depletion in some of these metabolites, you can see a flare in candida species. And if that dysbiotic state continues, so if the bacteria lose that ability to regain predominance in the gut, candida can continue. And will continue not only to predominate a lot more in that ecosystem, but it has the ability to gain access into the host and to look for nutrients in that host.
Claire Arrieta:
And it can make films in the gut. It can also become infectious. It can become septic too. And in fact, when we look at hosts as an example, immunocompromised hosts, or if we look at people that are in intensive care units, for example, and in many cases lose the barrier integrity, as well as immune components that will look after their defense of microorganisms. One very common septic organisms are candida, and other fungi as well. So yeah, when given the opportunity, they will look for resources inside of us instead of just the lumen of the gut.
Ruairi Robertson:
Really? But would you agree to say that they wouldn't cause a huge amount of gastrointestinal issues in day-to-day and in regular people, they're more associated with these kinds of severe infections? Or do you think they actually do have a role in things like IBS or maybe more severe conditions, IBD? Or is there evidence for that?
Claire Arrieta:
Yeah. Well, again, so in those inflammatory conditions, they definitely can have a role. There's really interesting work coming from the IBD field that have shown that the genetic predispositions that makes someone more likely to develop IBD, like the CARD9 genetic susceptibility, it's really directly involved in fungal immune recognition. So, that's actually what it does. It's common also to find flares of yeast, receding flares of IBD in Crohn's disease. And there's now really interesting work coming out showing that, yeah, indeed some of the immune responses associated with IBD are the same ones that are triggered by fungi and fungi can definitely aggravate it. So I think they do, of course, have a role in disease. Now, when we look at health, so if we look at a non-disease state, everyone has finger in their gut. It would be just like saying that that bacteria are implicated in inflammatory diseases. Of course they are. They're involved, now we know, even in cancer and the response to cancers. Just like bacteria, I think what we're going to find is a wide range of interactions between ourselves and the mechanisms that keep us homeostatic or healthy and those that don't. So, I think we'll find a bit of both.
Ruairi Robertson:
Right. And so, kind of on the flip side of the coin, you have these fungi which can potentially cause disease in certain circumstances, but there's certain fungi that actually have shown to be probiotic, per se. So, the one that's kind of commonly known, although somebody might've heard it, is a Saccharomyces boulardii. And that is often used as a probiotic alongside bacterial species. So, what do we know about that fungal probiotic and in what kind of conditions is it used for? Or does it have evidence for...
Claire Arrieta:
So, like with the majority of the probiotics, and this is a bit unfortunate, we only know kind of like the tip of the iceberg. We know in what conditions sometimes they're effective at battling or helping with a infection or a disease, but we know very little of how it's happening, or even if they're directly involved or indirectly involved in whatever result they may have. And we already used a good example of them. So, there's actually good studies of them showing that if they're given in addition to antibiotics, they reduce the risk of diarrhea that can be caused by antibiotics. So, lots of pediatricians use S. boulardii as well. And how it's happening, it's really not known, or at least I'm not aware of any studies that have shown whether it is that it becomes a member of the microbiome, and by doing so, it prevents pathogenic bacteria to taking hold, or if they produce a particular biochemical that will somehow balance the microbiome after it. It's really a big question mark. So we don't know how they work. We know that there's a lot of Saccharomyces normally, especially in babies, we find a lot of them. But what exactly they're doing, this is super early days for that.
Ruairi Robertson:
Wow. Well, you'll be finding about that soon, probably with all your new work. And so, you mentioned kind of babies, and I kind of want to finish off in this because that's where a lot of your work is at the moment. And you've shown before how the early life microbiome in babies may influence some immune mediated disorders, asthma and allergies. But there's not been a lot of work about how a fungi may play a role in this. So, what have you learned by this? How may fungi be educating the immune system in the gut to then affect a lung disorder such as asthma? What are the kind of processes that lead to that connection between fungi, the gut, and then the lung?
Claire Arrieta:
Yes. Well, there's actually quite a lot that we're interested now in that regard. Alluding to what I was saying before, fungi are pretty unique and distinct from bacteria from just the structural point of view, the building blocks of what makes their walls and different parts of their cells. And these different microbial patterns are recognized differently by the immune system. And we do know quite a bit. So, for example, chitin, which is part of their exo-structure and beta glucans, which is part of their membranes and the patterns that they package up and extra cellular vesicles, they have been studied for a while. Their immune responses have been studied for a while. And in many cases, what you're looking at are immune responses that are aligned with the type of inflammatory response that an asthmatic gets.
Claire Arrieta:
So, the classic asthmatic, the Th2, IgE mediated. Fungal patterns induce some of the same ones. And in fact, asthmatics in many cases, it's a very frequent allergy to respond to fungi in the environment. In many parts of the world, when it becomes really humid outside, and you see more and mold, and then you start to see more asthmatic attacks in the community. What we believe may be happening is that just like bacteria, fungi can be part of these early live education events that can prime the immune system to respond or not, strongly to many of these patterns of fungal structure. And this is some of what we're seeing now in babies. So, early in life, if you look at their microbiome, if you look at their fungi, there's a strong, and in many cases, stronger associations with those changes early in life, and then the risk to develop asthma later on.
Claire Arrieta:
So, the mechanisms of how this may be happening are pretty obscure right now. There's a very interesting study that allude to there being cross-immunity between some of the candida species that inhabits the guts, and the antibodies that react to spores that we inhale in the lung, for example. So, humeral cross-reactivity may be one of those mechanisms. That's the only one that has been described so far that can somewhat clearly explain the gut long axis, but I believe there's many. We're seeing that early in life, mice that have fungi versus mice that don't, have a different immune system. And that when given an antibiotic ,those animals that have fungi versus the ones that don't, have a stronger predisposition to overreact to long inflammation once they're given an antigen to do so.
Claire Arrieta:
So, I think that's strong evidence to show that yeah, fungi are definitely important early in life, and they can be more conducive to asthma, certain fungi, of course, only in certain individuals. I think they compliment the stories that have been published already from the bacteria. Fungi are definitely not the only contributor. We're looking at an ecosystem that contributes to immune education and the potential risks to an allergic disease. I think my argument is that we're better off if we study it together, than if we just kind of silo and only study fungi versus studying only bacteria.
Ruairi Robertson:
Yeah. It's all a whole ecosystem. So, how'd you see the future then, of the microbiome research? Do you see more fungal probiotics in the market? Do you see kind of treatments that target the fungal microbiome? Or do we learn more about the kind of metabolic output of fungal microbes in the gut? Or what do you see happening, or what would you like to see happening in the next few years to learn more about our fungal microbes?
Claire Arrieta:
I think that if we start including in those large studies, from microbiome observational studies to studies that are looking at therapies, if we start including fungi, we'll find out, as we have found out also, that they do have a role in impacting that ecosystem. So, if we want a more integral therapeutic or preventative that is going to target the microbiome, we're better off if we take into account the ecological role that these members of that ecosystem have. And if not, we may be missing out on a potential that we could harness by including them and what they may be doing. And in some cases, if we don't pay attention to them, we may perhaps miss collateral result that we're not expecting or hoping for, because we just decided to overlook the fungi. So, we were chatting before about their ability to overgrow. So it's important that whatever we're testing is also tested in the fungi and the role that they may have.
Ruairi Robertson:
So, thanks for listening to the Biomes podcast, sponsored by Microbiome Insights. My name is Dr. Ruairi Robertson. Tune in next time for some more exciting insights into latest developments in the human microbiome.