Holobiont

A holobiont is an assemblage of a host and the many other species living in or around it, which together form a discrete ecological unit through symbiosis, though there is controversy over this discreteness. The components of a holobiont are individual species or bionts, while the combined genome of all bionts is the hologenome. The holobiont concept was initially introduced by the German theoretical biologist Adolf Meyer-Abich in 1943, and then apparently independently by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation. The concept has evolved since the original formulations. Holobionts include the host, virome, microbiome, and any other organisms which contribute in some way to the functioning of the whole. Well-studied holobionts include reef-building corals and humans.

A holobiont is a collection of closely associated species that have complex interactions, such as a plant species and the members of its microbiome. Each species present in a holobiont is a biont, and the genomes of all bionts taken together are the hologenome, or the "comprehensive gene system" of the holobiont. A holobiont typically includes a eukaryote host and all of the symbiotic viruses, bacteria, fungi, etc. that live on or inside it.

Holobionts are distinct from superorganisms; superorganisms consist of many individuals, sometimes of the same species, and the term is commonly applied to eusocial insects. An ant colony can be described as a superorganism, whereas an individual ant and its associated bacteria, fungi, etc. are a holobiont. There is no doubt that symbiotic microorganisms are pivotal for the biology and ecology of the host by providing vitamins, energy and inorganic or organic nutrients, participating in defense mechanisms, or by driving the evolution of the host. There is still some controversy surrounding these terms, and they have been used interchangeably in some publications.

Holism is a philosophical notion first proposed by Aristotle in the 4th century BC. It states that systems should be studied in their entirety, with a focus on the interconnections between their various components rather than on the individual parts. Such systems have emergent properties that result from the behavior of a system that is "larger than the sum of its parts". However, a major shift away from holism occurred during the Age of Enlightenment when the dominant thought summarized as "dissection science" was to focus on the smallest component of a system as a means of understanding it.

The idea of holism started to regain popularity in biology when the endosymbiosis theory was first proposed by Konstantin Mereschkowski in 1905 and further developed by Ivan Wallin in 1925. Still accepted today, this theory posits a single origin for eukaryotic cells through the symbiotic assimilation of prokaryotes to form first mitochondria and later plastids (the latter through several independent symbiotic events) via phagocytosis (reviewed in Archibald, 2015). These ancestral and founding symbiotic events, which prompted the metabolic and cellular complexity of eukaryotic life, most likely occurred in the ocean.

Despite the general acceptance of the endosymbiosis theory, the term holobiosis or holobiont did not immediately enter the scientific vernacular. It was coined independently by the German Adolf Meyer-Abich in 1943, and by Lynn Margulis in 1990, who proposed that evolution has worked mainly through symbiosis-driven leaps that merged organisms into new forms, referred to as "holobionts", and only secondarily through gradual mutational changes. However, the concept was not widely used until it was co-opted by coral biologists over a decade later. Corals and the dinoflagellate algae called Zooxanthellae are one of the most iconic examples of symbioses found in nature; most corals are incapable of long-term survival without the products of photosynthesis provided by their endosymbiotic algae. Rohwer et al. (2002) were the first to use the word holobiont to describe a unit of selection in the sense of Margulis for corals, where the holobiont comprised the cnidarian polyp (host), Zooxanthellae algae, various ectosymbionts (endolithic algae, prokaryotes, fungi, other unicellular eukaryotes), and viruses.

Although initially driven by studies of marine organisms, much of the research on the emerging properties and significance of holobionts has since been carried out in other fields of research: the microbiota of the rhizosphere of plants or the animal gut became predominant models and have led to an ongoing paradigm shift in agronomy and medical sciences. Holobionts occur in terrestrial and aquatic habitats alike, and several analogies between these ecosystems can be made. For example, in all of these habitats, interactions within and across holobionts such as induction of chemical defenses, nutrient acquisition, or biofilm formation are mediated by chemical cues and signals in the environment, dubbed infochemicals. Nevertheless, we can identify two major differences between terrestrial and aquatic systems. First, water allows higher chemical connectivity and signaling between macro- and micro-organisms in aquatic or moist environments. In marine ecosystems, carbon fluxes also appear to be swifter and trophic modes more flexible, leading to higher plasticity of functional interactions across holobionts. Moreover, dispersal barriers are usually lower, allowing for faster microbial community shifts in marine holobionts. Second, phylogenetic diversity at broad taxonomic scales (i.e., supra-kingdom, kingdom and phylum levels), is higher in aquatic realms compared to land, with much of the aquatic diversity yet to be uncovered, especially marine viruses.

Host: The host member of a holobiont is typically a multicellular eukaryote, such as a plant or human. Notable hosts that are well-studied include humans, corals, and poplar trees.