https://www.sciencedirect.com/science/article/pii/S2452231719300181
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Highlights
Investigation of gut microbiome composition and diversity with respect to human personality.
Analyses targeted bacterial genera linked to behaviour in animal and human psychiatric studies.
Bacterial genera were modelled (using negative binomial regression) with respect to personality.
Genera linked to autism are also related to social behaviour in the general population.
Sociability is associated with higher diversity, and anxiety and stress with reduced diversity.
Abstract
The gut microbiome has a measurable impact on the brain, influencing stress, anxiety, depressive symptoms and social behaviour. This microbiome–gut–brain axis may be mediated by various mechanisms including neural, immune and endocrine signalling.
To date, the majority of research has been conducted in animal models, while the limited number of human studies has focused on psychiatric conditions. Here the composition and diversity of the gut microbiome is investigated with respect to human personality.
Using regression models to control for possible confounding factors, the abundances of specific bacterial genera are shown to be significantly predicted by personality traits. Diversity analyses of the gut microbiome reveal that people with larger social networks tend to have a more diverse microbiome, suggesting that social interactions may shape the microbial community of the human gut. In contrast, anxiety and stress are linked to reduced diversity and an altered microbiome composition. Together, these results add a new dimension to our understanding of personality and reveal that the microbiome–gut–brain axis may also be relevant to behavioural variation in the general population as well as to cases of psychiatric disorders.
1. Introduction
Personality shapes our world. It influences our health, our friendships, how we deal with stress, what jobs we succeed in and how we like to spend our time. It is approximately 50% heritable in human populations [1], suggesting that environmental factors also contribute significantly to our personality.
In addition to our external environment, the burgeoning field of the microbiome is revealing the many ways that our ‘environment within’ can affect our body’s physiology, including our digestion, immunity, metabolism, development and even our behaviour [2], [3], [4], [5], [6].
In fact, the number of microbial cells in our bodies is estimated to be roughly equal to our own human cells [7], with the majority of these microorganisms inhabiting the gut. Studies in the past decade provide evidence that the gut microbiome interacts with the central nervous system [8] and such findings have the potential to aid the development of new treatments for conditions such as autism [9] and depression [10]. However, research has largely been conducted in animal models and it is unknown how translatable these findings are to humans [11], [12], [13]. While there is some indication that dysbiosis of the gut microbiota may be implicated in neurological and psychiatric disorders [14], an open question remains as to whether variation in the gut microbial community is related to personality, that is behavioural differences between individuals that are consistent over time and different situations and therefore broadly predictable.
Animal studies have demonstrated that the gut microbiome can influence the stress response, anxiety and depressive-like behaviours, as well as social behaviour and communication [6], [15]. Some of the most convincing findings stem from faecal microbiota transplantation whereby behavioural traits can be transferred between mouse strains when their gut microbiota are swapped [16], [17].
For example, when the more anxious and timid Balb/c mice are colonized with the gut microbiota of NIH Swiss mice, their temperament becomes more bold and exploratory like that of the donor NIH Swiss mice, and vice versa [16]. Further support comes from the induction of anxiety and depressive-like behaviours in rodents colonized with the gut microbiota of humans suffering from these symptoms [18], [19], [20]. The transmission of such behaviours via the microbiota therefore suggests that gut microorganisms can contribute causally to behavioural traits. In fact, a recent human study reported improvement in psychiatric symptoms following faecal microbiota transplantation in patients with gastrointestinal disease [21].
There are numerous possible mechanisms that may mediate this interaction between the gut microbial community and the brain, including communication via neural, immune and endocrine pathways [6], [22], [23]. Microorganisms can also produce various neuroactive chemicals [24], [25] and can modulate host neurotransmitter levels [26]. For example, gut bacterial species such as those belonging to the genus Bacteroides have been shown to produce γ-aminobutyric acid (GABA) in large quantities in culture [27]. More recently it has been reported that the relative abundance of Bacteroides is negatively associated with brain signatures of depression [28], suggesting that bacterially derived GABA may play a role in the microbiome–gut–brain axis. Gut dysbiosis might lead to imbalances in neurotransmitters, inflammation or heightened activity of the hypothalamus–pituitary–adrenal axis that regulates the stress response [13]. The observation that psychiatric illnesses are often comorbid with gastrointestinal problems [29], [30] supports the role of the microbiome–gut–brain axis in human biology and psychology. A number of studies has reported associations between the composition of the gut microbiome and conditions such as autism, depression and schizophrenia (Table 1). However, results sometimes differ with regard to changes in the abundances of specific bacterial taxa, likely due to individual variability in gut microbiome composition together with underpowered studies. Furthermore, there is limited understanding of the mechanisms via which each of these bacterial taxa may affect the brain. Indeed, the predominant mechanism likely varies depending on the particular taxon involved, including anti-inflammatory effects, the production of short chain fatty acids, hormonal effects, the release of neuroactive metabolites including neurotransmitters and stimulation of the vagus nerve [23].
Table 1. Summary of statistically significant associations between bacterial genera in the gut and behavioural or psychiatric traits, as reported in the literature. Table lists findings from research in both animal models and human populations and includes all genera (23 in total) associated with these traits in at least two independent studies.
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Paper continued at: https://www.sciencedirect.com/science/article/pii/S2452231719300181
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