Tag Archives: Microbiota

Rheumatoid arthritis (RA)  is a complex, chronic inflammatory disease that is thought to affect about one percent of …

Rheumatoid arthritis (RA)  is a complex, chronic inflammatory disease that is thought to affect about one percent of the world’s population. RA happens when a person’s own antibodies attack joint tissue, causing painful swelling, stiffness, and redness. Some research has suggested that there is a link between RA and gum disease.

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Gum disease is estimated to affect up to 47 percent of adults, and in the disorder, oral microbes can move to the blood after the gums start to bleed. An increase in disease activity has been observed in RA patients who also have gum disease. Gum disease has been shown to be more common in RA patients who carry a certain type of antibodies, called anti-citrullinated protein antibodies (ACPAs), though ACPAs are often found in the blood of individuals with RA. The presence of ACPAs can often predate the diagnosis of RA by a few years.

A new study investigated the connections between these observations. In this work, the researchers collected blood samples from a small group of ten people with RA, five with and five without gum disease. These samples were collected every week for one year, and the investigators assessed the expression of both human and bacterial genes in those samples.

Certain types of inflammatory immune cells carried gene expression signatures that were associated with the autoimmune flares of arthritis patients who also had periodontal disease, as well as the presence of certain oral bacteria in the blood.

Many of these oral bacteria were chemically altered by deimination; they were citrullinated. Citrullination can change the structure and function of proteins. Although citrullination can be a part of the normal function of tissues, high levels of citrullination have been linked to inflammation.

Citrullination can also create targets for ACPAs; when the normal, unconverted forms of the oral bacteria were incubated with ACPAs, the antibodies did not react, but when the citrullinated oral bacteria were exposed to ACPAs, there was a reaction. ACPAs appear to be bound to oral microbes in RA patients.

The findings have been reported in Science Translational Medicine.

The study noted that the immune response to oral microbes could be influencing RA flares, that oral microbes can trigger a specific antibody reaction in patients with both RA and gum disease, and that RA flares cause varying immune signatures, which could reflect different flare triggers.

It could be that gum disease repeatedly causes the immune system to respond, and as the immune system keeps reacting and repeatedly increasing inflammation, RA may eventually begin to emerge. More work will be needed, however, to fully understand whether gum disease is playing a causative role in the development of RA.

Source: Science Translational Medicine

Carmen Leitch

For many years, there was debate about whether chronic fatigue syndrome was a ‘real’ disorder. It took time, …

For many years, there was debate about whether chronic fatigue syndrome was a ‘real’ disorder. It took time, but patients were eventually validated, and myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) was shown to be a disease that can cause various symptoms including fatigue, pain, cognitive difficulties, sleep problems, gastrointestinal issues, and post-exertional malaise. The causes of ME/CFS are still unclear and there is no way to treat it. But the gut microbiome has been shown to play a crucial role in many aspects of human health and disease, and now scientists have shown that the gut microbiomes of patients with myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) differ from those of healthy individuals. Two studies reported in Cell Host & Microbe have outlined these differences, showing that they might be used to diagnose ME/CFS. The gut microbiome may also present a treatment opportunity.

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In one of the studies, researchers assessed the gut bacteria of 106 people with ME/CFS and 91 healthy controls by analyzing stool samples. This research showed that the diversity of species, quantity of microbes, metabolic interactions, and relationships among the gut microbes were different from controls.

ME/CFS patients had unusually low levels of several types of bacteria, including Eubacterium rectale and Faecalibacterium prausnitzii, which generate the short-chain fatty acid butyrate. Previous research has shown that butyrate, a microbial metabolic byproduct, plays a crucial role in gut health maintenance. Butyrate provides a source of energy for cells lining the gut, aids in protecting the cells from disease, and supports the immune system in the gut.

Additional work showed that the reduction of certain bacteria levels was linked to decreases in butyrate production. With fewer butyrate-producing bacteria present, there were other species to fill the void. ME/CFS patients had higher levels of nine microbes, including two that have been linked to autoimmune disorders and inflammatory bowel disease – Enterocloster bolteae and Ruminococcus gnavus.

Symptoms of fatigue were found to increase as levels of F. prausnitzii decreased in ME/CFS patients, which suggests that disease severity may depend on gut microbe levels. People with ME/CFS also had low levels of a microbe that generates acetate.

Biochemical processes in the gut, which are influenced by relationships among gut microbes, were also notably different from controls; the bacterial network seems to be totally altered in ME/CFS patients.

The second report analyzed differences in the microbiomes of ME/CFS patients in different stages of disease. Health data, blood, and stool samples were analyzed from 149 ME/CFS patients; 74 of them had been diagnosed within the previous four years and were classified as short-term, while 75 had been diagnosed over a decade prior and were long-term. There were 74 healthy controls included in this work.

Those who were short-term had less diversity in their microbiomes and significantly lower levels of species that generate butyrate. Long-term patients had more stable microbiomes that were more similar to healthy controls, even while these individuals had more severe symptoms and worse metabolic disturbances. In all ME/CFS patients, tryptophan metabolism was decreased.

This work has shown that there could be biomarkers for ME/CFS in the microbiome, which could also help classify the disease and may lead to treatments, though a lot more research will be needed before those tests and treatments are realized.

Sources: National Institutes of Health, Cheng Guo et al Cell Host & Microbe 2023, Ruoyun Xiong et al Cell Host & Microbe 2023

Carmen Leitch

Gut feelings can be very real. There are neurons that connect the gut directly to the brain, and …

Gut feelings can be very real. There are neurons that connect the gut directly to the brain, and this so-called gut-brain axis has a significant influence on the body.
The microbes in the gut can also affect the brain, and researchers are trying to decipher the complex relationship between the brain and microorganisms in the body. Recent work has shown how microbial metabolites can influence brain function. Neurotransmitters can also affect gut physiology. Now scientists have developed a process that can be used by other researchers to develop a deep understanding of how gut microbes impact the brain. The work has been reported in Nature Protocols.

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“Currently, it is difficult to determine which microbial species drive specific brain alterations in a living organism,” said first study author, Dr. Thomas D. Horvath, an instructor at Baylor College of Medicine and Texas Children’s Hospital. “Here we present a valuable tool that enables investigations into connections between gut microbes and the brain.”

“Gut microbes can communicate with the brain through several routes, for example by producing metabolites, such as short-chain fatty acids and peptidoglycans; neurotransmitters, such as gamma-aminobutyric acid and histamine; and compounds that modulate the immune system as well as others,” added co-first study author Dr. Melinda A. Engevik, an assistant professor at the Medical University of South Carolina.

Related: Bugs on the Brain – Gut Microbes Affect Neurodegeneration

In this process, the researchers suggest creating a three-stage workflow. First, microbes should be prepared in a defined culture media. Next, intestinal organoids are injected with the microbes.  Finally, animal models are used that have either complete gut microbiomes; germ-free mice that lack microbiomes; mice that began as germ-free but were colonized with gut microbiota that carried no pathogens; and mice that started out germ-free but were colonized with individual strains of a gut microbe – Bifidobacterium dentium or Bacteroides ovatus.

The short-chain fatty acids produced by gut microbes can have a physiological impact on the brain, and they can be isolated and analyzed by  liquid chromatography–tandem mass spectrometry (LC/MS) along with any neurotransmitters that are derived from microbes.

This methodology is different from research that only assesses material in stool samples, because it encompasses many other things including in vivo models and cell cultures. The study authors estimated that the mouse colonization process requires about three weeks and LC/MS techniques take about another two weeks.

“We can expand our study to a community of microbes,” said study co-author Dr. Jennifer K. Spinler, an assistant professor at Baylor and the Texas Children’s Hospital Microbiome Center. “This protocol gives researchers a road map to understand the complex traffic system between the gut and the brain and its effects.”

Sources: Baylor College of Medicine, Nature Protocols

Carmen Leitch

The human gut microbiome exerts a significant influence on many aspects of our physiology. While it may not …

The human gut microbiome exerts a significant influence on many aspects of our physiology. While it may not be surprising that gut microbes can affect gut health, studies have also suggested that the gut microbiome can play a role in neurodegenerative diseases. What is less clear is whether those brain diseases are changing the microbes in the gut, or if gut microbes influence the health of the brain. New research has suggested that gut microbes generate molecules, such as short-chain fatty acids, that can exacerbate neurodegenerative conditions. The findings have been reported in Science.

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“We gave young mice antibiotics for just a week, and we saw a permanent change in their gut microbiomes, their immune responses, and how much neurodegeneration related to a protein called tau they experienced with age,” said senior study author David M. Holtzman, MD, a Professor at Washington University School of Medicine in St. Louis. “What’s exciting is that manipulating the gut microbiome could be a way to have an effect on the brain without putting anything directly into the brain.”

In this work, the researchers used a mouse model in which the animal are predisposed to brain damage that causes cognitive impairment. These mice express a mutated form of a protein called tau in the brain; tau tangles have been linked to neurodegenerative diseases including Alzheimer’s and Parkinson’s. In these mice, the mutant tau protein accumulates, as in disease, and causes the neurons of the brain to atrophy before the mice are 40 weeks old. These mice also carried a human APOE gene variant, APOE4, which is known to significantly increase the risk of Alzheimer’s.

When the researchers also ensured that these mice did not develop gut microbiomes by raising the germ-free mice in sterile conditions from birth, their brains acquired far less damage by 40 weeks compared to the same mice that were raised to have normal gut microbiomes.

If the mouse model with a microbiome was also given antibiotics when they were two weeks old, the composition of the bacterial species in their microbiomes was permanently altered. In male mice, this antibiotic-induced microbiome change was accompanied by a reduction in the brain damage that is typically seen at 40 weeks in these mice. Male mice that did not carry APOE4 also had more neuroprotection, potentially because the APOE4 variant may render some of the protection ineffective, suggested the researchers. Antibiotics did not affect neurodenegeration in female mice.

While researchers know that immune cells in male and female brains don’t respond to stimuli in the same way, the researchers don’t yet know what these findings mean for patients with neurodegeneration, noted Holtzman.

Additional work revealed that three specific short-chain fatty acids, generated by metabolic processes in some gut bacteria, are linked to neurodegeneration. There were only low levels of these fatty acids in mice with antibiotic-exposed gut microbiomes, and they were undetectable in mice lacking gut microbiomes – the mice with less brain damage.

The short-chain fatty acids may be triggering neurodegeneration by activating immune cells in circulation, which leads to immune cells in the brain to harm brain tissue. When mice lacking microbiomes consumed the three short-chain fatty acids, immune cells in the mouse brains became more reactive, and there were more signs of brain damage linked to tau.

The researchers are exploring whether modifications to the gut microbiome are a way to treat neurodegeneration.

In an unrelated study, scientists have also developed a new method for assessing interactions between the microbiome and the brain, which will help reveal more about this complex relationship and its health consequences.

Sources: Washington University School of Medicine, Science

Carmen Leitch

Our immune system is built to detect foreign invaders, pathogens, and debris, and then eliminate them. So how …

Our immune system is built to detect foreign invaders, pathogens, and debris, and then eliminate them. So how does it deal with the trillions of microbial cells that make a home for themselves in our gastrointestinal tract? Scientists have now found an answer to that question, and the evidence they revealed has also changed what we know about the interactions between immune receptors and a protein that helps move bacteria around, called flagellin. The findings have been reported in Science Immunology.

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There are many beneficial microbes in the human gut microbiome, and we need many of those microorganisms to help us break down food and absorb nutrients, for example. But there are also pathogenic gut germs. The immune system can recognize those pathogenic microbes with different receptors, one of which is called toll-like receptor 5 (TLR5). TLR5 attaches to flagellin, a protein found in the flagellum of bacteria, a structure that propels bacterial cells. When TLR5 binds to flagellin, an inflammatory response is triggered.

But many bacteria have flagellin, not only pathogens. Some bacteria have adapted and can make flagellin that will not bind to TLR5, so no immune response is initiated. But many harmless or so-called commensal bacteria generate flagellin that will still bind to TLR5. So how are these microbes tolerated by the immune system?

In this work, researchers delved deeply into flagellins, and analyzed those made by different bacteria. After assessing 116 flagellin proteins, they found that about half of them were not like any that were known; they could bind to TLR5 normally, but surprisingly, did not lead to an inflammatory response. The study authors have called these flagellin proteins “silent flagellins.” This has shown how the immune system tolerates commensal gut bacteria, even when those microbes share common features with pathogens.

This research has upended what we knew about TLR5 binding, which was once thought to be enough to trigger an inflammatory cascade.

“We now know that bacterial flagellin can interact with TLR5 at least three in different ways: bind and induce an immune response, bind and not induce an immune response, and evade by not binding,” noted senior study author Ruth Ley, director of the Department of Microbiome Science at the Max Planck Institute for Biology Tübingen.

“It is remarkable how tunable the response of the TLR5 receptor is,” added Ley.

After analyzing the genomes of many gut microbes, the researchers found that silent flagellins are a typical part of human gut microbes.

Sources: Max Planck Society, Science Immunology

Carmen Leitch

Humans carry around trillions of microbes in their gastrointestinal tracts, and research has shown that the gut microbiome …

Humans carry around trillions of microbes in their gastrointestinal tracts, and research has shown that the gut microbiome is closely linked to health. Studies have found that gut microbiomes are more healthy when they are made up of more diverse microbes, for example, and imbalances in the microbiome, or dysbiosis, is associated with disease. Scientists are now starting to look more closely at the specific types of microbes in the gut, and exactly how certain strains are influencing the development of specific disorders. A new report in Diabetes has identified two strains of gut microbes that seem to affect insulin sensitivity.

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A multitude of studies have associated the microbiome with metabolic disease. For example, research has indicated that people who have lower levels of bacteria that generate butyrate, a fatty acid, also don’t process insulin correctly.

In this new study, a bacterium called Coprococcus was found at higher levels in people who tended to have more sensitivity to insulin, while higher levels of a bacterium called Flavonifractor were found in those who tended to be less insulin sensitive. Coprococcus may be protecting people from type 2 diabetes while Flavonifractor could be promoting the development of type 2 diabetes.

But it’s also important to decipher whether microbes can cause disease, or if differences in the microbiome arise after the disease is present. Senior study author Mark Goodarzi, MD, Ph.D., the director of the Endocrine Genetics Laboratory at Cedars-Sinai, is also the principal investigator of a multicenter study called Microbiome and Insulin Longitudinal Evaluation Study (MILES), which is aiming to determine whether factors in the microbiome cause diabetes, or if diabetes changes the microbiome.

Since 2018, MILES researchers have been assessing data from Black and non-Hispanic white adults who are 40 to 80 years old. In this study, the focus was on 352 study volunteers who had not been diagnosed with diabetes. These volunteers gave stool samples, did glucose tolerance tests, and supplied other information such as data about dietary habits. In this group, 135 were found to have prediabetes and 28 people had glucose tolerance tests that met the threshold for a diabetes diagnosis.

The researchers examined 36 gut bacteria that generate butyrate in the study participants (from the stool samples), and found that Coprococcus and related bacteria are good for insulin sensitivity.

Although Flavonifractor also generates butyrate, it was associated with insulin resistance. This confirms previous research that has found higher Flavonifractor levels in diabetic people. These findings were significant after the researchers controlled for other factors that affect the development of diabetes, including sex, race, body mass index, and age.

The study authors cautioned, however that people should not yet try to change their microbiome to lower their risk of diabetes.

“As far as the idea of taking probiotics, that would really be somewhat experimental,” said Goodarzi. More research is needed to determine exactly which bacteria should be altered “… but it’s coming, probably in the next five to ten years.”

Now the researchers want to learn more about how diet changes the microbiome, and they are planning to follow up with study volunteers to learn more about changes in insulin resistance and the microbiome over time.

Sources: Cedars-Sinai Medical Center, Diabetes

Carmen Leitch

Microbes can easily share genes. Not only can different types of bacteria do this, there is also evidence …

Microbes can easily share genes. Not only can different types of bacteria do this, there is also evidence that entirely different branches of life – archaea and bacteria can also share genes. Some microbial genes can be found on small bits of DNA called mobile genetic elements, which are not a part of a microbe’s genome, but can still be expressed when they’re a microbial cell. These mobile genetic elements can move from one cell to another in a process known as horizontal gene transfer. Researchers have now found that bacteria in the maternal microbiome can share genes with bacteria in the infant microbiome, in the period just before birth until a few weeks after delivery – the perinatal period. Horizontal gene transfer enables maternal microbes to influence how bacteria in the infant microbiome are functioning, without actually moving the maternal microbes themselves. These findings have been reported in Cell.

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“This is the first study to describe the transfer of mobile genetic elements between maternal and infant microbiomes,” said senior study author Ramnik Xavier of the Broad Institute of MIT and Harvard. “Our study also, for the first time, integrated gut microbiome and metabolomic profiles from both mothers and infants and discovered links between gut metabolites, bacteria and breastmilk substrates. This investigation represents a unique perspective into the codevelopment of infant gut microbiomes and metabolomes under the influence of known maternal and dietary factors.”

The gut microbiome produces metabolites that can affect various aspects of infant development, such as immune system maturation and cognitive development during the perinatal period, a critical window. At birth, microbes move from the maternal microbiome to the infant microbiome, but we still have a lot to learn about how microbes are affecting development, and how they are developing into a microbiome themselves.

In this study, the researchers tracked the microbiomes and metabolites of 70 infant-mother pairs, from late pregnancy until the babies were one year old. This research showed that mobile genetic elements moved from microbes carried by moms and into microbes carried by infants. The mobile genetic elements that were transferred were often related to diet.

Infants were also found to have less diversity in their metabolomes compared to moms, however, there were metabolites, and links between microbes and metabolites that were identified exclusively by infants. Infants that got regular formula (that was not excessively hydrolyzed) also had metabolomes and cytokine signatures that were different from infants that were exclusively breastfed.

“The infant gut harbored thousands of unique metabolites, many of which were likely modified from breastmilk substrates by gut bacteria,” noted co-first study author Tommi Vatanen of the Broad Institute of MIT and Harvard. “Many of these metabolites likely impact immune system and cognitive development.”

This process seems to be a way for the maternal microbiome to exert an influence on the infant microbiome withouth transmitting specific species of bacteria.

Prophages, which are dormant bacteriophages, also seem to be involved in the movement of mobile genetic elements between the maternal and infant microbiomes, added Xavier.

Sources: Cell Press, Cell

Carmen Leitch

The microbes in our guts are closely connected to our brains, in a link known as the gut-brain …

The microbes in our guts are closely connected to our brains, in a link known as the gut-brain axis. Scientists have now found that a bacterium called HA-114 Lacticaseibacillus rhamnosus could help prevent amyotrophic lateral sclerosis (ALS). In a roundworm model of ALS, neurodegeneration was prevented by the microbe. The findings have been reported in Communications Biology.

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In ALS, the nerve cells that control movement, called motor neurons, gradually die off, causing a loss of movement and function. While the cause of ALS is still under investigation, this study has suggested that lipid metabolism disruptions are contributing to neurodegeneration, and HA-114 can provide protection against that deleterious influence.

Other research has also indicated that dysfunction in the gut microbiome may be involved in the development of ALS and other neurodegenerative disorders, noted lead study author Alex Parker, a Université de Montréal neuroscience professor.

When the researchers added the HA-114 microbe to the diet of the roundworm ALS model, motor neuron degeneration was suppressed, noted Parker. “The particularity of HA-114 resides in its fatty acid content.”

Roundworms called Caenorhabditis elegans have about 60 percent of their genome in common with humans and serve as common animal models. They carry some genes that have been linked to ALS.

Thirteen bacterial strains and three combinations of strains were tested on the worms. HA-114 had a significant impact, and reduced the motor disruption that occurs in models of both ALS and Huntington’s disease.

Additional work indicated that two genes, called acdh-1 and acs-20,  are involved in the neuroprotection provided by the bacteria. These genes are involved in the metabolism of fats, or lipids, and the breakdown of fatty acids for energy, a process called beta oxidation, which occurs in mitochondria.

Parker suggested that HA-114 is supplying fatty acids that enter mitochondria through a non-traditional pathway, which restores a balance in energy metabolism that becomes disrupted in ALS, and that decreases neurodegeneration.

The researchers are working on validating these findings in a mouse model of ALS, and are now planning to start a small clinical trial with ALS patients.

Sources: University of Montreal Hospital Research Centre, Communications Biology

Carmen Leitch

The microbes in the gut can metabolize some of the foods we eat to produce new molecules, some …

The microbes in the gut can metabolize some of the foods we eat to produce new molecules, some of which can affect our health. Researchers have previously shown that gut microbes can metabolize proteins in the diet to generate phenylacetylglutamine (PAG), a chemical that increases the risk of heart disease. New research has confirmed that link using human data, and expanded on what we know with an analysis of heart cells. The findings have been reported in Circulation: Heart Failure. This research may help scientists develop strategies to mitigate PAG-associated risks.

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This study assessed data from over 3,000 Americans and over 800 Europeans. It showed that increased PAG levels are linked to heart failure. Individuals with heart failure with preserved ejection fraction, in which there is a lack of heart muscle relaxation between beats, have elevated blood PAG levels, for example.

Blood PAG levels may serve to predict who is at risk for heart failure, suggested corresponding study author Stanley Hazen, M.D., Ph.D., department chair of Cardiovascular & Metabolic Sciences at the Lerner Research Institute. “The data build a strong case that making this test available for clinicians would add to their arsenal of diagnostic tests for heart failure.”

Hazen and colleagues reported that PAG can influence adrenergic receptors on platelets, which can affect things like blood clotting risks, in a study reported in Cell in 2020. That study is outlined in the video below.

This latest rsearch also showed that PAG and the parallel molecule found in mice, phenylacetylglycine, promote changes in gene expression and conditions that are related to heart failure, such as a reduction in contractility in certain heart cells.

Heart failure and cardiac disease is still a major cause of death around the world. Changes in diet that affect PAG levels may be one way to reduce the risk of heart disease.

“This study substantially expands the breadth of possible links between our diet and how our gut microbiome serves as a filter of our diet, impacting our susceptibility to develop different diseases,” said Hazen. “In this case, gut microbes form a metabolite from the amino acid phenylalanine in dietary protein, adversely impacting the function of a beating cardiac muscle cell.”

Hazen’s team is searching for the bacterium or bacteria and the enzymes they make that are involved in PAG production, and how to reduce PAG levels. Diet modifications might be a way to reduce risk too, added Hazen.

Sources: Cleveland Clinic, Circulation: Heart Failure

Carmen Leitch

Trillions of microbes live in our gastrointestinal tracts, and they are thought to exert a powerful influence on …

Trillions of microbes live in our gastrointestinal tracts, and they are thought to exert a powerful influence on various aspects of human biology, including mood. Studies have shown that there are associations between certain aspects of the gut microbiome and depression. We still don’t know much about how depression is caused on a biochemical level; research has indicated that genetics seem to only have a limited influence on the disease, for example. While there are treatments that can help some people, there are still millions of people with depression, and the disorder continues to be a leading cause of disability and mortality.

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Previous studieson depression and the microbiome have been small, done in animals, or have come to some conflicting conclusions, noted a new report in Nature Communications. This new research has expanded what we know about the gut microbiome and depression by taking a more careful approach; although this new work did not control for diet, which can be extremely difficult in human studies, it did control for medication use and lifestyle factors like exercise, weight, smoking, or drinking.

It was published with an accompanying study that investigated the microbiomes of a more diverse population as well. Data from 1,054 participants was used to find associations, which were then validated in another 1,539 individuals.

The research has shown that the microbiome and depression are connected, and that the composition of the microbiome is linked to the rates of depression in different ethnic groups. Data from the HELIUS study, which included 3,211 people, was used.

Microbiomes that lack certain species of bacteria, have fewer bacterial species in general – they are less diverse, were linked to a higher risk of depression or more symptoms of depression. This link was as statistically significant as other depression risk factors such as obesity, smoking, or a lack of exercise. While this research has not shown that factors in the microbiome cause depression, it has suggested that it may be possible to treat depression by modifying the microbiome.

The research revealed a consistent connection between depression and twelve bacterial groups, which all play a role in the production of neurotransmitters that have been related to depression, such as butyrate, glutamate, serotonin, and GABA.

“Now that we know which disturbances in the microbiome are significant for depression, this opens up new possibilities for treatment and prevention. Which is urgently needed,” said Anja Lok, a senior author of one of the studies and researcher at Amsterdam UMC.

“The substantial ethnic differences in depression do indeed appear to be related to ethnic differences in the microbiome. We don’t know exactly why this is yet,” noted a corresponding author of one of the studies, Jos Bosch, a researcher from the University of Amsterdam. “This association was not caused by differences in lifestyle such as smoking, drinking, weight or exercise, and merits further investigation. For example, diet could play a role.”

Sources: University of Amsterdam, Bosch et al Nature Communications 2022, Radjabzadeh et al Nature Communications 2022

Carmen Leitch