Hologenome theory of evolution

The hologenome theory of evolution, also known as the hologenome concept of evolution, recasts the individual animal or plant (and other multicellular organisms) 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 (i.e., an integrated social unit composed of conspecifics), 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.

In 1991, Lynn Margulis coined the term holobiont in a book chapter entitled Symbiogenesis and Symbionticism in Symbiosis as a Source of Evolutionary Innovation: Specation and Morphogenesis (MIT Press). The term holobiont is derived from the Ancient Greek (hólos, “whole”), and the word biont for a unit of living matter.

In September 1994, Richard Jefferson first introduced the term hologenome at a presentation at Cold Spring Harbor Laboratory during a Symposium "A Decade of PCR", published by Cold Spring Harbor Laboratory Press as a video series. At the CSH Symposium and earlier, the unsettling number and diversity of microbes that were being discovered through the powerful tool of PCR-amplification of 16S ribosomal RNA genes was exciting, but confusing interpretations in diverse studies. A number of speakers referred to microbial contributions to mammalian or plant DNA samples as 'contamination'. In his lecture, Jefferson argued that these were likely not contamination, but rather essential components of the samples that reflected the actual genetic composition of the organism being studied, and that the logic of the organism's performance and capabilities would be embedded only in the hologenome. Observations on the ubiquity of microbes in plant and soil samples as well as laboratory work on molecular genetics of vertebrate-associated microbial enzymes informed this assertion (citations needed).

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