Holobiont

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.[1][7] 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.[8] A holobiont typically includes a eukaryote host and all of the symbiotic viruses, bacteria, fungi, etc. that live on or inside it.[7]

Holobionts are distinct from superorganisms; superorganisms consist of many individuals, sometimes of the same species, and the term is commonly applied to eusocial insects.[9][10] An ant colony can be described as a superorganism, whereas an individual ant and its associated bacteria, fungi, etc. are a holobiont.[8] 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.[11][12] There is still some controversy surrounding these terms, and they have been used interchangeably in some publications.[6]

Host: The host member of a holobiont is typically a multicellular eukaryote, such as a plant or human.[8] Notable hosts that are well-studied include humans,[13]</ref> corals,[5] and pine trees.[14]

Microbiome: The microbiome includes bacteria,[3] archaea,[15] microscopic fungi,[7] and microscopic protists.[3] 

Virome: All of the viruses included in a holobiont are collectively referred to as the virome[16]

Fungi: Multicellular fungi can be included in holobionts, such as arbuscular mycorrhizal fungi (AMF) in the roots of plants.[7][4]

The holobiont phenotype [2]

Holobionts are entities composed of a host and all of its symbiotic microbes.[2]

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.[2]

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 (white). 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.[2]

Recent years have seen the development of powerful but relatively inexpensive tools for characterising microbial communities, including high throughput sequencing technologies such as whole genome shotgun sequencing. These technological advances have resulted in an explosion of interest in microbial ecology and in the evolution of microbe-host relationships. Some researchers question whether the holobiont concept is needed, and whether it does justice to the intricacies of host-symbiont relationships.[30] In 2016 Douglas and Werren took issue with the concept that "the holobiont (host plus its microbiome) and its constituent hologenome (the totality of genomes in the holobiont) are a unit of selection, and therefore this unit has properties similar to an individual organism".[31] 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 (the holobiont), 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."[31]

The holobiont and by extension the hologenome concept remain controversial, particularly in regard to the host and its microbiome as a single evolutionary unit.[32] 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.[32]

Nevertheless, the holobiont concept has resulted in a shift from the focus on symbioses involving one microbial partner and a single host (squids and luminescent Aliivibrio, legumes and Rhizobium, aphids and Buchnera) toward a greater interest in symbioses in complex multi-partner consortia (animal gut systems, marine invertebrates, plant and seaweed epiphytes, microbe-microbe interactions in soil, aquatic biomes).[32] 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,[33] expanding host plant usage[34] and temperature adaptation.[35][32]

• Hologenomics
• Hologenome theory of evolution
• Phytobiome
• Pan-genome
• Superorganism