Eating for 3.8 × 1013: Examining the Impact of Diet and Nutrition on the Microbiota-Gut-Brain Axis Through the Lens of Microbial Endocrinology

Abstract

The study of host-microbe neuroendocrine crosstalk, termed microbial endocrinology, suggests the impact of diet on host health and microbial viability is, in part, reliant upon nutritional modulation of shared host-microbe neuroendocrine axes. In the 1990's it was first recognized that neuroendocrine pathways are major components of the microbiota-gut-brain axis, and that diet-induced changes in the gut microbiota were correlated with changes in host behavior and cognition. A causative link, however, between nutritional-induced shifts in microbiota composition and change in host behavior has yet to be fully elucidated. Substrates found in food which are utilized by bacteria in the production of microbial-derived neurochemicals, which are structurally identical to those made by the host, likely represent a microbial endocrinology-based route by which the microbiota causally influence the host and microbial community dynamics via diet. For example, food safety is strongly impacted by the microbial production of biogenic amines. While microbial-produced tyramine found in cheese can elicit hypertensive crises, microorganisms which are common inhabitants of the human intestinal tract can convert L-histidine found in common foodstuffs to histamine and thereby precipitate allergic reactions. Hence, there is substantial evidence suggesting a microbial endocrinology-based role by which the gastrointestinal microbiota can utilize host dietary components to produce neuroactive molecules that causally impact the host. Conversely, little is known regarding the reverse scenario whereby nutrition-mediated changes in host neuroendocrine production affect microbial viability, composition, and/or function. Mechanisms in the direction of brain-to-gut, such as how host production of catecholamines drives diverse changes in microbial growth and functionality within the gut, require greater examination considering well-known nutritional effects on host stress physiology. As dietary intake mediates changes in host stress, such as the effects of caffeine on the hypothalamic-pituitary-adrenal axis, it is likely that nutrition can impact host neuroendocrine production to affect the microbiota. Likewise, the plasticity of the microbiota to changes in host diet has been hypothesized to drive microbial regulation of host food preference via a host-microbe feedback loop. This review will focus on food as concerns microbial endocrinology with emphasis given to nutrition as a mediator of host-microbe bi-directional neuroendocrine crosstalk and its impact on microbial viability and host health.

First step of odorant detection in the olfactory epithelium and olfactory preferences differ according to the microbiota profile in mice

“…This result reinforces the idea that the microbiota during the juvenile period is important for the development of normal odor preference [33]. Olfactory preferences are also essential in feeding behaviour [34] and the diversity of food ingested has an impact on the microbiota [33,35]. Our present work indicates that the microbiota could play a key role in shaping the chemical senses and thus the feeding behaviour of mammals as it has recently been shown in insects [36][37][38][39].…”

“…A preference for male odor by female mice was only observed in the germfree mice inoculated with mice microbiota. This result reinforces the idea that the microbiota during the juvenile period is important for the development of normal odor preference [33]. Olfactory preferences are also essential in feeding behaviour [34] and the diversity of food ingested has an impact on the microbiota [33,35].…”

“…Purified amplicons were sequenced using the MiSeq sequencing technology (Illumina, San Diego, CA, USA) at the GeT-PLaGe platform (Genotoul, Toulouse, France). Paired-end reads obtained from MiSeq sequencing were analyzed using the Galaxy supported pipeline named Find RapidlyOperational Taxonomic Units (OTUs) with Galaxy Solution (FROGS) (33). For the preprocessing, only reads with length ≥380 bp were kept.…”

Dialog between skin and its microbiota: Emergence of “Cutaneous Bacterial Endocrinology”

“…[16] In addition, food itself contains neuroendocrine factors and precursors, which can directly act on the intestinal microbiota. [17] The skin harbours the second most abundant microbiome of the human body in terms of mass and diversity. [18] As the gut, skin is a major neuroendocrine organ [19,20] innervated by a dense network of nerve fibres [20] and in constant interaction with the environment.…”

Pyruvate is required for catecholamine-stimulated growth of different strains of Campylobacter jejuni

“…Microbial endocrinology is an emerging field of research that studies the bidirectional communication between host and microbiota in which neurochemicals serve as a common language shared between both (Lyte, 2016b). As an interdisciplinary research area, the theoretical framework can be employed to examine mechanisms that may be involved in the ability of stress to influence the pathogenesis of infectious disease (Lyte, 2016b;Lyte, 2019). In the present study, we employed a microbial endocrinology-based approach to examine the effect(s) of stress-related catecholamines on C. jejuni growth.…”