Holobiont

Holobionts are assemblages of different species that form ecological units. Lynn Margulis proposed that any physical association between individuals of different species for significant portions of their life history is a symbiosis. All participants in the symbiosis are bionts, and therefore the resulting assemblage was first coined a holobiont by Lynn Margulis in 1991 in the book Symbiosis as a Source of Evolutionary Innovation.[1] Holo is derived from the Ancient Greek word ὅλος (hólos) for “whole”. The entire assemblage of genomes in the holobiont is termed a hologenome.

History

In 1992, David Mindell subsequently used the word holobiont in a BioSystems article in general reference to host-microbe symbioses.[2] This was followed in 1993 by its use in another BioSystems article by R. Jorgensen.[3] The word rested dormant for about a decade. Forest Rohwer, Victor Seguritan, Farooq Azam, and Nancy Knowlton adopted the term in a figure legend to describe the complex relationships between various microbes and coral in 2002.[4] In this system, the zooxanthellae determine the light level required by the coral holobiont and a complicated web involving the Bacteria, Archaea and fungi recycles its nitrogen. The word holobiont has been increasingly used since then, with its next appearance in 2005.[5] It has been popularized by the hologenome concept.[6] All macrobes, animals and plants, are today deemed holobionts consisting of the host plus its entire microbial community,[7][8][9][10] and these associations can be transient or stable.[11][12][13]

Relationship to viromes and microbiomes

Holobionts are traditionally divided into three major divisions: 1) viruses, 2) unicellular microbes and 3) the macrobial host. Collectively, the viruses make up the virome and microbes make up the microbiome. There is no specific terminology for other multicellular organisms associated with the holobiont other than symbiont. The collective genomic DNA and RNA of a holobiont is called a hologenome.

Versus hologenome

Holobionts are considered multipartite ecological entities, whereas hologenomes are multigenomic entities that encode holobiont phenotypes. Here, the word hologenome follows a conceptual continuum from words such as chromosome and genome. The terms are therefore structural definitions relating to host-microbial assemblages and their genomes.

Versus superorganism

Superorganisms are organisms consisting of many individuals and was first applied to the eusocial insects (Wheeler 1928).[14] An ant colony is a superorganism. Holobionts are assemblages of many different species. Each ant is an individual holobiont consisting of the ant, fungi, bacteria, etc. However, ″superorganism″ has also been used as a synonym for ″Holobiont″.[15]

Criticism

Some authors reject the concept since they consider is far from encompassing most of host-symbiont relationships to make it justifiable. They would also argue that symbionts do not necessarily co-evolve with the host.[16]

See also

References

  1. ↑ "Symbiosis as a Source of Evolutionary Innovation". MIT Press. Retrieved 2016-08-12.
  2. ↑ Mindell, D. P. (1992-01-01). "Phylogenetic consequences of symbioses: Eukarya and Eubacteria are not monophyletic taxa". Bio Systems. 27 (1): 53–62. ISSN 0303-2647. PMID 1391691.
  3. ↑ Jorgensen, R. (1993-01-01). "The origin of land plants: a union of alga and fungus advanced by flavonoids?". Bio Systems. 31 (2–3): 193–207. ISSN 0303-2647. PMID 8155852.
  4. ↑ Rohwer, Forest; Seguritan, Victor; Azam, Farooq; Knowlton, Nancy (2002-11-13). "Diversity and distribution of coral-associated bacteria". Marine Ecology Progress Series. 243: 1–10. doi:10.3354/meps243001.
  5. ↑ Baruch, Rinkevich; Avishai, Nanthawan; Rabinowitz, Claudette (2005-03-01). "UV incites diverse levels of DNA breaks in different cellular compartments of a branching coral species". The Journal of Experimental Biology. 208 (Pt 5): 843–848. doi:10.1242/jeb.01496. ISSN 0022-0949. PMID 15755882.
  6. ↑ Rosenberg, Eugene; Koren, Omry; Reshef, Leah; Efrony, Rotem; Zilber-Rosenberg, Ilana (2007-05-01). "The role of microorganisms in coral health, disease and evolution". Nature Reviews. Microbiology. 5 (5): 355–362. doi:10.1038/nrmicro1635. ISSN 1740-1534. PMID 17384666.
  7. ↑ Gordon, Jeffrey; Youle, Merry; Knowlton, Nancy; Rohwer, Forest; Relman, David A. (2013-04-01). "Superorganisms and Holobionts". Microbe Magazine. 8 (4): 152–153. doi:10.1128/microbe.8.152.1. ISSN 1558-7452.
  8. ↑ 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.
  9. ↑ 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.
  10. ↑ Agler, Matthew T.; Ruhe, Jonas; Kroll, Samuel; Morhenn, Constanze; Kim, Sang-Tae; Weigel, Detlef; Kemen, Eric M. (2016-01-20). "Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation". PLOS Biol. 14 (1): e1002352. doi:10.1371/journal.pbio.1002352. ISSN 1545-7885. PMC 4720289. PMID 26788878.
  11. ↑ Theis, Kevin R.; Dheilly, Nolwenn M.; Klassen, Jonathan L.; Brucker, Robert M.; Baines, John F.; Bosch, Thomas C. G.; Cryan, John F.; Gilbert, Scott F.; Goodnight, Charles J. (2016-04-26). "Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes". mSystems. 1 (2): e00028–16. doi:10.1128/mSystems.00028-16. ISSN 2379-5077.
  12. ↑ Rosenberg, Eugene; Zilber-Rosenberg, Ilana (2016-05-04). "Microbes Drive Evolution of Animals and Plants: the Hologenome Concept". mBio. 7 (2): e01395–15. doi:10.1128/mBio.01395-15. ISSN 2150-7511. PMC 4817260. PMID 27034283.
  13. ↑ Hester, ER; Barott, KL; Nulton, J; Vermeij, MJ; Rohwer, FL (May 2016). "Stable and sporadic symbiotic communities of coral and algal holobionts". The ISME Journal. 10 (5): 1157–69. doi:10.1038/ismej.2015.190. PMID 26555246.
  14. ↑ Wheeler, WM (1928). The Social Insects, Their Origin and Evolution. Harcourt Brace.
  15. ↑ 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. Free, full text.
  16. ↑ 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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