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. The components of a holobiont are individual species or, while the combined genome of all bionts is the hologenome. The concept of the holobiont was defined by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation. Holobionts include the host, virome, microbiome, and other members, all of which contribute in some way to the function of the whole. Well-studied holobionts include reef-building corals and humans.
However, there is controversy over whether holobionts can be viewed as single evolutionary units.

Overview

A holobiont is a collection of species that are closely associated and 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. However, there is still some controversy surrounding these terms, and they have been used interchangeably in some publications.

Holobiont components

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 pine trees.
Microbiome: The microbiome includes bacteria, archaea, microscopic fungi, and microscopic protists. 
Virome: All of the viruses included in a holobiont are collectively referred to as the virome
Fungi: Multicellular fungi can be included in holobionts, such as arbuscular mycorrhizal fungi in the roots of plants.

The holobiont phenotype

Holobionts are entities composed of a host and all of its symbiotic microbes.
In the diagram, the symbiotic microbes that affect a holobiont's phenotype and have coevolved with the host are coloured blue, while those which affect the holobiont’s phenotype but have not coevolved with the host are coloured red. Those that do not affect the holobiont’s phenotype at all are coloured gray. Microbes may be transmitted vertically or horizontally, may be acquired from the environment, and can be constant or inconstant in the host.
It follows that holobiont phenotypes can change in time and space as microbes come into and out of the holobiont. Microbes in the environment are not part of the holobiont. Hologenomes then encompass the genomes of the host and all of its microbes at any given time point, with individual genomes and genes falling into the same three functional categories of blue, red, and gray. Holobionts and hologenomes are entities, whereas coevolution or the evolution of host-symbiont interactions are processes.

Examples

In corals

Reef-building corals are holobionts that include the coral itself, photosynthetic dinoflagellates called zooxanthellae, and associated bacteria and viruses. Co-evolutionary patterns exist for coral microbial communities and coral phylogeny.

In plants

The plant holobiont is relatively well-studied, with particular focus on agricultural species such as legumes and grains. Bacteria, fungi, archaea, protists, and viruses are all members of the plant holobiont.
The bacteria phyla known to be part of the plant holobiont are Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria. For example, nitrogen-fixers such as Azotobacter and Bacillus greatly improve plant performance.
Fungi of the phyla Ascomycota, Basidiomycota, and Glomeromycota colonize plant tissues and provide a variety of functions for the plant host. Arbuscular mycorrhizal fungi, for instance, are common across plant groups and provide improved nutrient acquisition, temperature and drought resistance, and reduced pathogen load. Epichloë species are part of the meadow fescue holobiont and provide herbivore resistance by producing ergot alkaloids, which cause ergotism in mammals.
Protist members of the plant holobiont are less well-studied, with most knowledge oriented towards pathogens. However, there are examples of commensalistic plant-protist associations, such as Phytomonas.

Gallery

Controversy

Recent years have seen the development of powerful but relatively inexpensive tools for characterising microbial communities, such as high throughput sequencing technologies. These technological advances have resulted in an explosion of interest in microbial ecology and the evolution of microbe-host relationships. However some researchers question whether the holobiont concept is needed, and whether it does justice to the intricacies of host-symbiont relationships. In 2016 Douglas and Werren took issue with the concept that "the holobiont and its constituent hologenome are a unit of selection, and therefore this unit has properties similar to an individual organism". They argue that "the hologenome concept is unhelpful to the study of host interactions with resident microorganisms because it focuses on one level of selection, and as a result it is concerned with cooperative and integrative features of host-microbe systems to the exclusion of other kinds of interactions, including antagonism among microorganisms and conflicts between host and microbial partners."
The holobiont and by extension the hologenome concept remain controversial, particularly in regard to the host and its microbiome as a single evolutionary unit. In order to validate the holobiont concept from an evolutionary perspective, new theoretical approaches are needed that acknowledge the different levels at which natural selection can operate in the context of microbiome-host interactions. For example, selection could occur at the level of the holobiont when a transgenerational association among specific host and symbiont genotypes can be maintained.
Nevertheless, the holobiont concept has resulted in a shift from the focus on symbioses involving one microbial partner and a single host toward a greater interest in symbioses in complex multi-partner consortia. Moreover, there is a realization that even the relatively well understood binary symbioses such as aphids and Buchnera are more complex with a number of diverse facultative symbionts contributing to resistance to parasites, expanding host plant usage and temperature adaptation.