Functions of the Microbiota for the Physiology of Animal Metaorganisms

Abstract

Animals are usually regarded as independent entities within their respective environments. However, within an organism, eukaryotes and prokaryotes interact dynamically to form the so-called metaorganism or holobiont, where each partner fulfils its versatile and crucial role. This review focuses on the interplay between microorganisms and multicellular eukaryotes in the context of host physiology, in particular aging and mucus-associated crosstalk. In addition to the interactions between bacteria and the host, we highlight the importance of viruses and nonmodel organisms. Moreover, we discuss current culturing and computational methodologies that allow a deeper understanding of underlying mechanisms controlling the physiology of metaorganisms.

Keywords: Host; Metaorganism; Microbiome; Microbiota; Physiology.

Fig. 1

Functional interactions in metaorganisms. All eukaryotic organisms live in a close and interdependent relationship with their microbiome, including bacteria, viruses, and other small eukaryotes, and are therefore regarded as metaorganisms. Members of the microbiome have various functions within the metaorganism. Microorganisms contribute to host development, organ morphogenesis, metabolism, aging, behavior, colonization resistance, pathogen protection, and maturation of the immune system. Dysbiosis or imbalances in these homeostatic host-microbiome interactions are associated with various diseases including anxiety, depression, diabetes, cancer, obesity, and chronic inflammation.

Fig. 2

Interactions between the intestinal mucus and the microbiome. The intestinal mucus layer serves as an interface of the host with the microbiota and also represents a specific niche. The species composition differs between intestinal lumen and mucus. Mucus-consuming bacteria colonize the mucus layer and use mucins as an energy source. Products of these metabolic activities, such as tryptophan or its metabolites, are then provided to the host and widely affect its physiology. Microorganisms can also influence mucus production or host immune responses and thereby shape the intestinal habitat.

Fig. 3

Molecular changes of intestinal host-microbiome interactions during aging. Upon birth the newborn is colonized by environmental microorganisms. Microbial diversity increases and stabilizes until adulthood. In the elderly, microbiome diversity increases further, presumably due to loss of regulatory processes. Moreover, bacterial composition and microbiome functions change in the elderly. The relative abundance of bacteria that trigger inflammatory responses increases, whereas functional processes involved in DNA repair as well as production of cobalamin, biotin, and β-glucuronidases decrease in the elderly microbiome. In contrast, bacteria which are involved in creatine degradation and polysaccharide utilization increase in the elderly. These changes in the microbiome over the course of an individual's life therefore impact on metabolism and inflammatory processes, which in turn affect disease susceptibility and development.