Holobiont

Part of a series on
Microbiomes
Plant microbiomes Endosphere Phyllosphere Rhizosphere laimosphere root microbiome soil microbiome spermosphere
Marine microbiomes Seagrass Coral Cetacean Marine microbial symbiosis
Human microbiomes Human milk Fecal transplant Gut–brain axis Placental Salivary Uterine Necrobiome
Other microbiomes Mycobiome Phycosphere Built environment Drosophila gut
Microbiota Plant endophyte epiphyte rhizobacteria Human gut lung oral skin vaginal Marine Microbial community Initial acquisition Accessible carbohydrates Flora (microbiology)
Holobionts Plant holobiont Marine holobiont coral crab seagrass sponge rhodolith Hologenomics hologenome evolution
Viromes Bat Human Mangrove Viriome Virosphere
Related Biomass partitioning Dysbiosis Gnotobiosis Phytobiome Quorum sensing Biological dark matter Microbial population biology Microbial cooperation Metagenomics viral Metatranscriptomics Metabolomics Pan-genome Superorganism Symbiogenesis
Projects Human Microbiome Project Earth Microbiome Project
Category
v t e

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,^[2] 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,^[3] and then apparently independently by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation.^[2] The concept has evolved since the original formulations.^[4] Holobionts include the host, virome, microbiome, and any other organisms which contribute in some way to the functioning of the whole.^[5][6] Well-studied holobionts include reef-building corals and humans.^[7][8]

Overview

A holobiont is a collection of closely associated species that have complex interactions, such as a plant species and the members of its microbiome.^[2][9] 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.^[10] A holobiont typically includes a eukaryote host and all of the symbiotic viruses, bacteria, fungi, etc. that live on or inside it.^[9]

Holobionts are distinct from

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.^[15][16] 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.^[17]

The idea of holism started to regain popularity in biology when the

Host: The host member of a holobiont is typically a multicellular eukaryote, such as a plant or human.^[10] Notable hosts that are well-studied include humans,^[41] corals,^[7] and poplar trees.^[42]

Microbiome: The microbiome includes bacteria,^[5] archaea,^[43] microscopic fungi,^[9] and microscopic protists.^[5] 

Virome: All of the viruses included in a holobiont are collectively referred to as the virome^[44]

Fungi: Multicellular fungi can be included in holobionts, such as arbuscular mycorrhizal fungi (AMF) in the roots of plants.^[9][6]

The holobiont phenotype

Holobionts are entities composed of a host and all of its symbiotic microbes.^[4]

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.^[4]

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.^[4]

Plants

Although most work on host-microbe interactions has been focused on animal systems such as corals, sponges, or humans, there is a substantial body of literature on plant holobionts.^[45] Plant-associated microbial communities impact both key components of the fitness of plants, growth and survival,^[6] and are shaped by nutrient availability and plant defense mechanisms.^[9] Several habitats have been described to harbor plant-associated microbes, including the rhizoplane (surface of root tissue), the rhizosphere (periphery of the roots), the endosphere (inside plant tissue), and the phyllosphere (total above-ground surface area).^[14] The holobiont concept originally suggested that a significant fraction of the microbiome genome together with the host genome is transmitted from one generation to the next and thus can propagate unique properties of the holobiont".^[46] In this regard, studies have shown that seeds can play such a role. Evidence of this process have been recently proven showing that the majority, up to 95%, of the seed microbiome is mistranslated across generations.^[47]

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.^[5]

The bacteria phyla known to be part of the plant holobiont are

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 (Trypanosomatidae).^[50]

Marine

Reef-building corals are holobionts that include the coral itself (a eukaryotic invertebrate within class Anthozoa), photosynthetic dinoflagellates called zooxanthellae (Symbiodinium), and associated bacteria and viruses.^[7] Co-evolutionary patterns exist for coral microbial communities and coral phylogeny.^[51]

• 
  Coral holobiont^[52]
• 
  Seagrass holobiont^[14]
• 
  Sponge holobiont^[53]
• 
  Climate change and the rhodolith holobiont^[54]

Effects of stressors

Effects of stressors on the holobiont

The holobiont response to stressors

Stressors can alter directly the host physiology and immunity, and the symbiotic community composition and density. Stressors may also indirectly affect the symbiotic community by altering the host physiology (which represents the symbiotic niche), and the immune state of the host. Conversely, symbionts can buffer stressors via nutrient provision, physiological tolerance, and defense against host natural enemies.^[55]

The holobiont response to stressors is difficult to predict, as many factors can be under selection. This includes host resistance genes and plastic mechanisms, but also acquisition of symbionts that can constitute a pool of genes with new functions. Some key factors that can preferentially select for the host or the symbionts to adapt to stressors are: (1) the features of the stressor, such as its frequency or amplitude, but also its combination with another stressor that can lead to an additive, synergistic or antagonist interaction; (2) the transmission mode of the symbionts; (3) the specificity and the efficiency of the given buffering mechanism, and the net balance between its cost and its benefit.^[55]

Holobiomics

Holobiomics is the scientific analysis of a community of holobionts, which focuses on the interconnections between its components in the context of the prevailing environmental conditions rather than on the individual parts. The scientific approach for this emerging research field is based on the concept of holism. Holobiomics aims to study the holobionts of a system, their properties, and their interactions in their entirety.

The term "holobiomics" is composed of Greek elements όλος (hólos), "all, whole, total", and βίος (bíos), "life", ending on -ome (biome); and the suffix -omics (-ομική, feminine), which identifies subfields of modern biology that aim at the characterisation and quantification of the entirety of similar individual elements in order to draw conclusions about the structure, function, and dynamics of a system.

To infer the properties and interactions of the symbiotic partners, techniques in molecular biology,^[56] ecology,^[57] and modelling^[58] are combined.

Controversy

Recent years have seen the development of powerful but relatively inexpensive tools for characterising microbial communities, including

The holobiont and by extension the hologenome concept remain controversial, particularly in regard to the host and its microbiome as a single evolutionary unit.[61] 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.^[61]

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

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

References