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.[1] The components of a holobiont are individual species or bionts, 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[1]. Holobionts include the host, virome, microbiome, and other members, all of which contribute in some way to the function of the whole[2][3]. Well-studied holobionts include reef-building corals and humans[4][5].

Definition

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][6]. 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[7]. A holobiont typically includes a eukaryote host and all of the symbiotic viruses, bacteria, fungi, etc. that live on or inside it[6].

Versus Superorganism

Holobionts are distinct from superorganisms; superorganisms consist of many individuals, sometimes of the same species, and the term is commonly applied to eusocial insects[8][9]. An ant colony can be described as a superorganism, whereas an individual ant and its associated bacteria, fungi, etc. are a holobiont[7]. However, there is still some controversy surrounding these terms, and they have been used interchangeably in some publications[5].

Components of the Holobiont

Host

The host member of a holobiont is typically a multicellular eukaryote, such as a plant or human[7]. Notable hosts that are well-studied include humans[10], corals[4], and pine trees[11].

Microbiome

The microbiome includes bacteria[2], archaea[12], microscopic fungi[6], and microscopic protists[12].  

Virome

All of the viruses included in a holobiont are collectively referred to as the virome[13].

Fungi

Multicellular fungi can be included in holobionts, such as arbuscular mycorrhizal fungi (AMF) in the roots of plants[6][3].

In corals

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[4]. Co-evolutionary patterns exist for coral microbial communities and coral phylogeny.[14]

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[12].

The bacteria phyla known to be part of the plant holobiont are Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria[2] . For example, nitrogen-fixers such as Azotobacter (Proteobacteria) and Bacillus (Firmicutes) greatly improve plant performance[2].

Fungi of the phyla Ascomycota, Basidiomycota, and Glomeromycota colonize plant tissues and provide a variety of functions for the plant host[12]. Arbuscular mycorrhizal fungi (Glomeromycota), for instance, are common across plant groups and provide improved nutrient acquisition, temperature and drought resistance, and reduced pathogen load[15]. Epichloë species (Ascomycota) are part of the meadow fescue holobiont and provide herbivore resistance by producing ergot alkaloids, which cause ergotism in mammals[16].

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)[17].

Criticism

Some authors reject the holobiont concept, saying it does not sufficiently encompass the intricacies of host-symbiont relationships[18].

See also

References
  1. Margulis, Lynn; Fester, René. "Symbiosis as a Source of Evolutionary Innovation". MIT Press. Retrieved 2016-08-12.
  2. Bulgarelli, Davide, Klaus Schlaeppi, Stijn Spaepen, Emiel Ver Loren van Themaat, and Paul Schulze-Lefert. “Structure and Functions of the Bacterial Microbiota of Plants.” Annual Review of Plant Biology 64, no. 1 (2013): 807–38. https://doi.org/10.1146/annurev-arplant-050312-120106.
  3. Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie; Le Van, Amandine; Dufresne, Alexis (2015-06-01). "The importance of the microbiome of the plant holobiont". The New Phytologist. 206 (4): 1196–1206. doi:10.1111/nph.13312. ISSN 1469-8137. PMID 25655016.
  4. Knowlton, Nancy, and Forest Rohwer. “Multispecies Microbial Mutualisms on Coral Reefs: The Host as a Habitat.” The American Naturalist 162, no. 4 Suppl (October 2003): S51-62. https://doi.org/10.1086/378684.
  5. Kramer, Peter; Bressan, Paola (2015). "Humans as superorganisms: How microbes, viruses, imprinted genes, and other selfish entities shape our behavior". Perspectives on Psychological Science. 10 (4): 464–481. doi:10.1177/1745691615583131. ISSN 1745-6916. PMID 26177948. Free, full text.
  6. Sánchez-Cañizares, Carmen, Beatriz Jorrín, Philip S Poole, and Andrzej Tkacz. “Understanding the Holobiont: The Interdependence of Plants and Their Microbiome.” Current Opinion in Microbiology, Mobile genetic elements and HGT in prokaryotes * Microbiota, 38 (August 1, 2017): 188–96. https://doi.org/10.1016/j.mib.2017.07.001.
  7. Bordenstein, Seth R.; Theis, Kevin R. (2015-08-18). "Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes". PLOS Biol. 13 (8): e1002226. doi:10.1371/journal.pbio.1002226. ISSN 1545-7885. PMC 4540581. PMID 26284777.
  8. Youle, Merry, Nancy Knowlton, Forest Rohwer, Jeffrey Gordon, and David A. Relman. “Superorganisms and Holobionts: Looking for a Term for the Functional Entity Formed by a Macrobe and Its Associated Symbiotic Microbes and Viruses? The Term Is ‘Holobiont.’” Microbe Magazine 8, no. 4 (April 1, 2013): 152–53. https://doi.org/10.1128/microbe.8.152.1.
  9. Wheeler, WM (1928). The Social Insects, Their Origin and Evolution. Harcourt Brace.
  10. Guchte, Maarten van de, Hervé M. Blottière, and Joël Doré. “Humans as Holobionts: Implications for Prevention and Therapy.” Microbiome 6, no. 1 (December 2018): 81. https://doi.org/10.1186/s40168-018-0466-8.
  11. Hacquard, Stéphane, and Christopher W. Schadt. “Towards a Holistic Understanding of the Beneficial Interactions across the Populus Microbiome.” New Phytologist 205, no. 4 (March 2015): 1424–30. https://doi.org/10.1111/nph.13133.
  12. Hassani, M. Amine, Paloma Durán, and Stéphane Hacquard. “Microbial Interactions within the Plant Holobiont.” Microbiome 6, no. 1 (March 27, 2018): 58. https://doi.org/10.1186/s40168-018-0445-0.
  13. Grasis, Juris A. “The Intra-Dependence of Viruses and the Holobiont.” Frontiers in Immunology 8 (November 9, 2017). https://doi.org/10.3389/fimmu.2017.01501.
  14. Pollock, F. Joseph; McMinds, Ryan; Smith, Styles; Bourne, David G.; Willis, Bette L.; Medina, Mónica; Thurber, Rebecca Vega; Zaneveld, Jesse R. (2018-11-22). "Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny". Nature Communications. 9 (1): 1–13. doi:10.1038/s41467-018-07275-x. ISSN 2041-1723.
  15. Begum, Naheeda, Cheng Qin, Muhammad Abass Ahanger, Sajjad Raza, Muhammad Ishfaq Khan, Muhammad Ashraf, Nadeem Ahmed, and Lixin Zhang. “Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance.” Frontiers in Plant Science 10 (2019). https://doi.org/10.3389/fpls.2019.01068.
  16. Guerre, Philippe. “Ergot Alkaloids Produced by Endophytic Fungi of the Genus Epichloë.” Toxins 7, no. 3 (March 6, 2015): 773–90. https://doi.org/10.3390/toxins7030773.
  17. Schwelm, Arne, Julia Badstöber, Simon Bulman, Nicolas Desoignies, Mohammad Etemadi, Richard E. Falloon, Claire M. M. Gachon, et al. “Not in Your Usual Top 10: Protists That Infect Plants and Algae.” Molecular Plant Pathology 19, no. 4 (October 11, 2017): 1029–44. https://doi.org/10.1111/mpp.12580.
  18. Moran, Nancy A.; Sloan, Daniel B. (2015-12-04). "The Hologenome Concept: Helpful or Hollow?". PLOS Biology. 13 (12): e1002311. doi:10.1371/journal.pbio.1002311. ISSN 1545-7885. PMC 4670207. PMID 26636661.
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