Box 2 | A proposal — the hologenome theory of evolution

From the following article:

The role of microorganisms in coral health, disease and evolution

Eugene Rosenberg, Omry Koren, Leah Reshef, Rotem Efrony & Ilana Zilber-Rosenberg

Nature Reviews Microbiology 5, 355-362 (May 2007)

doi:10.1038/nrmicro1635

The theory is based on the following well-established empirical data:

  • All animals and plants establish symbiotic relationships with microorganisms. Often the number of microorganisms and their combined genetic information far exceeds that of their host cells. We refer to the host and its symbiont population as the holobiont, and the host genome and the genomes of all the symbiotic microorganisms as the hologenome.
  • Different host species contain different symbiont populations and individuals of the same species can also contain different symbiont populations. Therefore, genotypic and phenotypic variation exists between hosts of the same species and between their microbiota.
  • The association between a host organism and its microbial community affect both the host and its microbiota; the nature of the interaction can range from mutualism through commensalism to that of a pathogenic interaction.
  • The genetic information encoded by microorganisms can change under environmental demands more rapidly, and by more processes, than the genetic information encoded by the host organism. There are at least three mechanisms by which the genetic information encoded by a microbial population that is symbiotically associated with a host can change: first, by alterations in the relative abundance of microorganisms currently associated with the host; second, through the introduction of new microorganisms from the environment; and third, by genetic alteration of the existing microbial population through mutation, horizontal gene transfer and subsequent selection. Each of these mechanisms is more versatile and can occur in a much shorter timeframe than the alteration and selection processes required for host genome evolution.

In summary, the genome of the host can act in consortium with the genomes of the associated symbiotic microorganisms to create a hologenome. This hologenome — given the diversity and fast growth rates of microorganisms — can change more rapidly than the host genome alone, thereby conferring greater adaptive potential to the combined holobiont organism.

Each of these points taken together lead us to propose a hologenome theory of evolution: the holobiont with its hologenome should be considered as the unit of natural selection in evolution, and microbial symbionts have an important role in adaptation and evolution of higher organisms. Therefore, microorganisms are essential not only in the health and disease of individual higher organisms, but they also are a significant factor in species survival and evolution.

This hologenome theory of evolution is derived primarily from an understanding of the biology of corals. However, a large body of data exists in the literature relating to many eukaryotic organisms and their interaction with symbiotic microorganisms — a literature that could be re-evaluated in light of this theory.