Editorial: Epigenetics as a Deep Intimate Dialogue between Host and Symbionts

摘要

Host-symbiont epigenetic crosstalk: A “ koiné language” that enables communication between different species In ancient Greek, the term koiné refers to a common language, which spread in the Eastern Mediterranean region and the Near East following the conquests of Alexander the Great. In the 4th century BC, koiné quickly became a shared language that enabled people speaking different dialects to communicate with each other. Indeed, effective communication is always necessary for overcoming “barriers” between individuals and groups, tightening relationships, and enabling new ways of coping with a changing world. This is the case not only for interactions involving cultural relations. Different living entities communicate in many ways, with the most intimate and often the most long-lasting communication being the formation of mutually beneficial, obligatory symbiotic associations. As Lynn Margulis forcefully argued, symbiotic relations are found among virtually all living organisms, and were critical for the origin and diversification of the eukaryotes (Sagan, 1967 ; Margulis, 1971 ; Guerrero et al., 2013 ). Since the partners in symbiotic relationships frequently belong to different kingdoms, and the intimacy may be so deep that the Symbionts reside in the tissues and/or cells of the host, their shared “language” should be a basic—and ancient—form of communication. Such effective communication blurs the boundaries between different living entities, giving rise to a single biomolecular network, a “holobiont” with a “hologenome” (Zilber-Rosenberg and Rosenberg, 2008 ; Bordenstein and Theis, 2015 ), thus problematizing the conventional notion of individuality. The series of papers presented in this topic-issue explore the fascinating developmental and evolutionary relationship between Symbionts and hosts, by focusing on the mediating epigenetic processes that enable the communication to be effective and robust at both the individual, the ecological, and the evolutionary time scales. One of the currently most researched cases illustrating the productive cross-talk between Symbionts and hosts is the symbiosis between mammals and their gut microbiome. As Gilbert stresses, the birth of a mammal is not merely the origin of a new distinct (traditional) individual, but the onset of a new community. Already in utero , the fetus interacts with a network of symbiotic factors that is provided by the mother and, at birth, as it leaves the maternal symbiotic association system, it forms its own community which, although largely based on the legacy it gets from its mother, becomes rapidly adapted to its specific idiosyncratic conditions of life. Since the normal development and the thriving of the newborn depend on the symbiotic legacy it receives, it is the holobiont—the community of interacting species—that is the target of both developmental and natural selection. However, as Fridmann-Sirkis et al. illustrate, in extreme circumstances, when interactions fail, for example, because of acute stress to the microbiome, the host adapts by making adaptive changes in its epigenome, which can be inherited by subsequent generations. In more normal conditions, the maternal legacy provides crucial developmental resources, and is the basis on which flexible, context-sensitive, modifications of these resources, that allow rapid adaptation to the normally dynamic and fluctuating conditions in which the new individual lives, are constructed. Since the microbiome reacts and evolutionarily adapts much faster than the host, most host's physiological adaptations are likely to be initiated by evolutionary changes to the constitution of the microbiome. Soen analyzes the manner in which the changes in the constitution of the microbiome lead to the modification of the communication process among the species comprising the microbiome, as well as between the microbiome and the host; and shows how these changes enable the developmental construction of a new dynamic, adaptive equilibrium, involving mutually beneficial epigenetic modifications in the host that can be epigenetically inherited between host generations. Hence, adaptive evolutionary modifications in the rapidly evolving microbiome, that occur at the time scale of host's individual life, are followed by the epigenetic inheritance of the host's physiological adaptations, thus enabling adaptive adjustments of the host at the ecological time scale ( Soen ; see also Moran and Sloan, 2015 ). Although many symbiotic associations play essential roles in host development, physiology, and health, some associations may be harmful for the host. In these cases, the “selfish” Symbiont (often referred to as “parasite”) must evade the host's immune responses, and this may occur through “misleading” the host, for example, by mimicking the host's signaling and control system for its own benefits. Some intracellular pathogenic bacteria, such as Anaplasma phagocytophilum a pathogen studied by Sinclair et a