Holobiont

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Microbiome relationships mirror host evolution. The more distantly related species are, the more distinct the composition of their cognate microbiomes, as reflected in the overlaid phylogeny of wasps and their microbiota. Microbiome relationships mirror host evolution.png
Microbiome relationships mirror host evolution. The more distantly related species are, the more distinct the composition of their cognate microbiomes, as reflected in the overlaid phylogeny of wasps and their microbiota.

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]

Contents

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 superorganisms; superorganisms consist of many individuals, sometimes of the same species, and the term is commonly applied to eusocial insects. [11] [12] An ant colony can be described as a superorganism, whereas an individual ant and its associated bacteria, fungi, etc. are a holobiont. [10] 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. [13] [14] There is still some controversy surrounding these terms, and they have been used interchangeably in some publications. [8]

History of the holobiont concept

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 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). [18] These ancestral and founding symbiotic events, which prompted the metabolic and cellular complexity of eukaryotic life, most likely occurred in the ocean. [19] [17]

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, [20] [21] 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. [22] [23] 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) [24] were the first to use the word holobiont to describe a unit of selection sensu Margulis [25] for corals, where the holobiont comprised the cnidarian polyp (host), Zooxanthellae algae, various ectosymbionts (endolithic algae, prokaryotes, fungi, other unicellular eukaryotes), and viruses. [17]

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. [26] [27] [28] 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. [29] [30] [31] [32] Nevertheless, we can identify two major differences between terrestrial and aquatic systems. First, the physicochemical properties of water result in 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. [33] Moreover, dispersal barriers are usually lower, allowing for faster microbial community shifts in marine holobionts. [34] [35] Secondly, 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, [36] [37] especially marine viruses. [38] [39] [40] [17]

Holobiont components

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

The holobiont phenotype The holobiont phenotype.jpg
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 Actinomycetota, Bacteroidota, Bacillota, and Pseudomonadota. [5] For example, nitrogen-fixers such as Azotobacter (Pseudomonadota) and Bacillus (Bacillota) greatly improve plant performance. [5]

Fungi of the phyla Ascomycota, Basidiomycota, Glomeromycota, and Mucormycotina colonize plant tissues and provide a variety of functions for the plant host. [5] Arbuscular mycorrhizal fungi (Glomeromycota), for instance, are common across plant groups and provide improved nutrient acquisition, temperature and drought resistance, and reduced pathogen load. [48] Epichloë species (Ascomycota) are part of the meadow fescue holobiont and provide herbivore resistance by producing ergot alkaloids, which cause ergotism in mammals. [49]

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]

Effects of stressors

Effects of stressors on the holobiont.jpg
Effects of stressors on the holobiont
Factors that can influence the holobiont stress response.jpg
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

Visual depiction of a holobiont: a human and their microbiome Holobiont representation.png
Visual depiction of a holobiont: a human and their microbiome

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 led to 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. [59] 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". [60] 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." [60]

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 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). [61] 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, [62] expanding host plant usage [63] and temperature adaptation. [64] [61]

See also

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

<span class="mw-page-title-main">Symbiosis</span> Close, long-term biological interaction between distinct organisms (usually species)

Symbiosis is any type of a close and long-term biological interaction between two biological organisms of different species, termed symbionts, be it mutualistic, commensalistic, or parasitic. In 1879, Heinrich Anton de Bary defined it as "the living together of unlike organisms". The term is sometimes used in the more restricted sense of a mutually beneficial interaction in which both symbionts contribute to each other's support.

<span class="mw-page-title-main">Coral</span> Marine invertebrates of the class Anthozoa

Corals are colonial marine invertebrates within the class Anthozoa of the phylum Cnidaria. They typically form compact colonies of many identical individual polyps. Coral species include the important reef builders that inhabit tropical oceans and secrete calcium carbonate to form a hard skeleton.

Joan Roughgarden is an American ecologist and evolutionary biologist. She has engaged in theory and observation of coevolution and competition in Anolis lizards of the Caribbean, and recruitment limitation in the rocky intertidal zones of California and Oregon. She has more recently become known for her rejection of sexual selection, her theistic evolutionism, and her work on holobiont evolution.

Symbiotic bacteria are bacteria living in symbiosis with another organism or each other. For example, rhizobia living in root nodules of legumes provide nitrogen fixing activity for these plants.

Horizontal transmission is the transmission of organisms between biotic and/or abiotic members of an ecosystem that are not in a parent-progeny relationship. This concept has been generalized to include transmissions of infectious agents, symbionts, and cultural traits between humans.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

<span class="mw-page-title-main">Marine microorganisms</span> Any life form too small for the naked human eye to see that lives in a marine environment

Marine microorganisms are defined by their habitat as microorganisms living in a marine environment, that is, in the saltwater of a sea or ocean or the brackish water of a coastal estuary. A microorganism is any microscopic living organism or virus, that is too small to see with the unaided human eye without magnification. Microorganisms are very diverse. They can be single-celled or multicellular and include bacteria, archaea, viruses and most protozoa, as well as some fungi, algae, and animals, such as rotifers and copepods. Many macroscopic animals and plants have microscopic juvenile stages. Some microbiologists also classify viruses as microorganisms, but others consider these as non-living.

The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts. For recent literature on holobionts and hologenomes published in an open access platform, see the following reference.

<span class="mw-page-title-main">Root microbiome</span> Microbe community of plant roots

The root microbiome is the dynamic community of microorganisms associated with plant roots. Because they are rich in a variety of carbon compounds, plant roots provide unique environments for a diverse assemblage of soil microorganisms, including bacteria, fungi, and archaea. The microbial communities inside the root and in the rhizosphere are distinct from each other, and from the microbial communities of bulk soil, although there is some overlap in species composition.

<span class="mw-page-title-main">Microbiome</span> Microbial community assemblage and activity

A microbiome is the community of microorganisms that can usually be found living together in any given habitat. It was defined more precisely in 1988 by Whipps et al. as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity". In 2020, an international panel of experts published the outcome of their discussions on the definition of the microbiome. They proposed a definition of the microbiome based on a revival of the "compact, clear, and comprehensive description of the term" as originally provided by Whipps et al., but supplemented with two explanatory paragraphs. The first explanatory paragraph pronounces the dynamic character of the microbiome, and the second explanatory paragraph clearly separates the term microbiota from the term microbiome.

<span class="mw-page-title-main">Marine microbial symbiosis</span>

Microbial symbiosis in marine animals was not discovered until 1981. In the time following, symbiotic relationships between marine invertebrates and chemoautotrophic bacteria have been found in a variety of ecosystems, ranging from shallow coastal waters to deep-sea hydrothermal vents. Symbiosis is a way for marine organisms to find creative ways to survive in a very dynamic environment. They are different in relation to how dependent the organisms are on each other or how they are associated. It is also considered a selective force behind evolution in some scientific aspects. The symbiotic relationships of organisms has the ability to change behavior, morphology and metabolic pathways. With increased recognition and research, new terminology also arises, such as holobiont, which the relationship between a host and its symbionts as one grouping. Many scientists will look at the hologenome, which is the combined genetic information of the host and its symbionts. These terms are more commonly used to describe microbial symbionts.

<span class="mw-page-title-main">Eugene Rosenberg</span>

Eugene Rosenberg is a microbiologist at the Faculty of Life Sciences at Tel Aviv University, an expert in the field of applied environmental microbiology, in particular his work on Myxobacteria, microorganisms to combat pollution (bioremediation), and the Hologenome theory of evolution.

<span class="mw-page-title-main">Mycobiome</span> The fungal community in and on an organism

The mycobiome, mycobiota, or fungal microbiome, is the fungal community in and on an organism.

Hologenomics is the omics study of hologenomes. A hologenome is the whole set of genomes of a holobiont, an organism together with all co-habitating microbes, other life forms, and viruses. While the term hologenome originated from the hologenome theory of evolution, which postulates that natural selection occurs on the holobiont level, hologenomics uses an integrative framework to investigate interactions between the host and its associated species. Examples include gut microbe or viral genomes linked to human or animal genomes for host-microbe interaction research. Hologenomics approaches have also been used to explain genetic diversity in the microbial communities of marine sponges.

Vertical transmission of symbionts is the transfer of a microbial symbiont from the parent directly to the offspring. Many metazoan species carry symbiotic bacteria which play a mutualistic, commensal, or parasitic role. A symbiont is acquired by a host via horizontal, vertical, or mixed transmission.

<span class="mw-page-title-main">Marine microbiome</span>

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

<span class="mw-page-title-main">Plant microbiome</span>

The plant microbiome, also known as the phytomicrobiome, plays roles in plant health and productivity and has received significant attention in recent years. The microbiome has been defined as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity".

<span class="mw-page-title-main">Plant holobiont</span>

Since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a holobiont. Selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. However, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments.

<span class="mw-page-title-main">Marine holobiont</span>

The holobiont concept is a renewed paradigm in biology that can help to describe and understand complex systems, like the host-microbe interactions that play crucial roles in marine ecosystems. However, there is still little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them and their ecological consequences. The holobiont concept posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution.

References

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