Eco-Evolutionary Dynamics of the Human-Gut Microbiota Symbiosis in a Changing Nutritional Environment

Abstract

The operational harmony between living beings and their circumstances, their ever-changing environment, is a constitutive condition of their existence. Nutrition and symbiosis are two essential aspects of this harmony. Disruption of the symbiosis between host and gut microbiota, the so-called dysbiosis, as well as the inadequate diet from which it results, contribute to the etiology of immunometabolic disorders. Research into the development of these diseases is highly influenced by our understanding of the evolutionary roots of metabolic functioning, thereby considering that chronic non-communicable diseases arise from an evolutionary mismatch. However, the lens has been mostly directed toward energy availability and metabolism, but away from our closest environmental factor, the gut microbiota. Thus, this paper proposes a narrative thread that places symbiosis in an evolutionary perspective, expanding the traditional framework of humans’ adaptation to their food environment.

The Metabolic Syndrome, a Human Disease

“…This refers to the Lamarckian adaptations of live human beings-and, especially, of their descendants-to the conditions of the medium and their genetic [494,495] (but mainly epigenetic [496,497]) modulation. The implication of the diverse niches of the human microbiota has extended our horizons to the modulation not only of our cells and tissues, but also to the commensal, symbiotic, and even parasitic cells that do not share our DNA but live within us and are a necessary part of us (as a biocenosis) [498,499]. The transfer and handling of cell organelles (mainly mitochondria, so far) may be contemplated within this context of tissue structure, function, and cell composition shifting [482,[500][501][502].…”

Oral microbiota of patients with phenylketonuria: A nation‐based cross‐sectional study

“…In contrast, the health-beneficial properties of microbial communities that evolved with an ancestral diet can be attributed to the production of beneficial metabolites influencing pH, re-mineralizing enamel, regulating inflammation or contributing to maintain a protective biofilm (Franck et al, 2022). At this time, comprehensive studies on the interaction between diet, microbiome and oral health are scarce, likely due to logistical challenges in long-term dietary interventions.…”

“…In contrast, the health‐beneficial properties of microbial communities that evolved with an ancestral diet can be attributed to the production of beneficial metabolites influencing pH, re‐mineralizing enamel, regulating inflammation or contributing to maintain a protective biofilm (Franck et al, 2022).…”

Food System Transformation and Gut Microbiota Transition: Evidence on Advancing Obesity, Cardiovascular Diseases, and Cancers—A Narrative Review

“…With innovative dietary practices, the vital mutualism between the human host and its bacterial symbionts may change, possibly affecting the immune system and intestinal barrier functions [ 28 ]. For example, throughout evolution, the primary source of food for primates was plants [ 29 ]. This suggests that certain species and metabolic functions within gut bacterial ecosystems, as well as individuals able to benefit from their presence and functions, may have been preferentially selected [ 30 , 31 , 32 , 33 ].…”

“…Therefore, the evolution of primate-microbiota symbiosis may have shaped the genetic structure of the host immune system and digestive tract to enable a tolerogenic response towards microbial ecosystems suitable for ecological niches created by a significant amount of plant consumption, as well as to respond appropriately to stimuli generated from those, in order to ensure their containment inside the gut [ 34 , 35 , 36 , 37 ]. Therefore, it can be believed that a food system dietary setting composed primarily of ripe and unripe fruits, young leaves, flowers, seeds, and, at times, roots and tubers would have chosen the most suitable individuals to tolerate microbial species able to create ecosystems equipped with enzymatic repertoires adapted to the degradation of the majority of the non-digestible elements of this diet [ 29 ]. In fact, a sizeable amount of the health advantages of a plant diet are linked to the modification of the gut microbiota [ 38 , 39 ].…”