Microbial regulation of organismal energy homeostasis

Abstract

Facts and figures on the gut microbiota The term microbiota refers to all the microorganisms present in the various ecosystems in the human body. Diverse communities of microorganisms are located throughout the human body, including the gut, lungs, vaginal and urinary tracts and skin. The microbiota is composed of several types of microbes: bacteria, archaea, viruses, phages, yeast and fungi 1. Humans have constantly coevolved in the presence of these microorganisms, thereby establishing symbiotic relationships. Several lines of evidence suggest that in addition to bacteria, other types of microbes, such as fungi, protozoa and viruses, also have important interactions with the human in which they reside, referred to as the host in this review 2,3. Nevertheless, interactions between bacteria and human cells have been studied the most and will be the focus of this review. The human body carries approximately 3.9 × 10 13 bacterial cells, with the largest amount residing in the large intestine: 10 11 bacteria cells g-1 of wet stool 4. At the most recent estimation, almost 10 million non-redundant microbial genes have been identified in the human gut 5. This number is 150-fold higher than the number of genes in the human genome 6. Therefore, the metabolic capacity of the gut microbiota greatly exceeds the metabolic capacity of human cells. The theory of energy harvest Pioneering studies linking SCFAs and energy harvest. The complex and dynamic ecosystem of the gut microbiota contributes to the metabolism of various compounds, thereby leading to the production of numerous metabolites. In the early 2000s, pioneering studies from Gordon and colleagues 11 linked the production of specific metabolites, such as short-chain fatty acids (SCFAs), to host energy homeostasis (Table 1). Bäckhed et al. 12 demonstrated the role of the gut microbiota in host energy metabolism and growth by showing that germ-free mice gained less body weight and fat mass than conventionalised mice (that is, those harbouring a gut microbiota). This difference was observed despite increased food intake in germ-free mice. The same group of researchers found that the microbiota of genetic obese mice (ob/ob) harvests more energy than their lean ob/+ counterparts. In addition, this phenotype was transferred in germ-free mice transplanted with the microbiota from the obese donors 11. Initially, the hypothesis was that this shift provided more SCFAs (acetate, propionate, butyrate and lactate) that could be used as metabolic substrates by the host (Fig. 1). In addition, it was suggested that the gut microbiota contributed to energy metabolism through a direct interaction with the digestive tract. Indeed, the germ-free mice exhibit a lower level of caecal SCFAs than

Inter‐organ communication: a gatekeeper for metabolic health

“…In addition, Mills and colleagues demonstrated that succinate accumulates in BAT upon cold exposure and favors thermogenesis in an UCP1-dependent manner [164]. Furthermore, gut microbiota has been described in the past two decades as a very important player in the regulation of whole-body energy homeostasis, in response to diverse stimuli such as cold [165,166], nutrition [167,168], or fasting/feeding cycles [168][169][170], through the production of mediators such as short chain fatty acids (SCFAs) and secondary BAs [167,169].…”

“…Furthermore, gut microbiota has been described in the past two decades as a very important player in the regulation of whole‐body energy homeostasis, in response to diverse stimuli such as cold , nutrition , or fasting/feeding cycles , through the production of mediators such as short chain fatty acids (SCFAs) and secondary BAs .…”

Measurement of gut microbial metabolites in cardiometabolic health and translational research

“…The gut microbiota is composed of trillions of microorganisms inhabiting the intestines. In recent years, the interactions between gut microbes and host have been shown to influence many physiological responses, including energy metabolism, immune maturation, and neurodevelopment in the human body . The imbalance of gut microbiota, known as dysbiosis, has also been revealed to correlate with numerous human disease phenotypes .…”

“…In recent years, the interactions between gut microbes and host have been shown to influence many physiological responses, including energy metabolism, immune maturation, and neurodevelopment in the human body. [1][2][3][4] The imbalance of gut microbiota, known as dysbiosis, has also been revealed to correlate with numerous human disease phenotypes. 5,6 Notably, the effects of gut microbiota are only not confined to the intestine but can systemically contribute to human disease and health.…”

Potential correlation between carbohydrate‐active enzyme family 48 expressed by gut microbiota and the expression of intestinal epithelial AMP‐activated protein kinase β

“…For example, SCFAs induced by fiber-enriched diets play important roles in the microbiotagut-brain communication pathway, through the regulation of appetite, energy homeostasis, and maintenance of the intestinal barrier function(Byrne, Chambers, Morrison, & Frost, 2015;Cani et al, 2019).Interestingly, with the exception of an alteration in gut microbiota composition, different microbial CAZyme gene family profiles and AMPK β levels were observed between the groups. Specifically, two genera, Dubosiella and Bacillus, were significantly more abundant in the RM group, which could contribute to ecological dysbiosis and, consequently, colon inflammation.…”