The hologenome theory 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.
Origin
Lynn Margulis coined the term holobiont in her 1991 book Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis (MIT Press), though this was not in the context of diverse populations of microbes. The term holobiont is derived from the Ancient Greek ὅλος (hólos, "whole"), and the word biont for a unit of life.
In September 1994, Richard Jefferson coined the term hologenome when he introduced the hologenome theory of evolution at a presentation at Cold Spring Harbor Laboratory.Number 6 in a series of 7 VHS recordings, A Decade of PCR: Celebrating 10 Years of Amplification, Cold Spring Harbor Laboratory Press, 1994. . http://www.cshlpress.com/default.tpl?.Part 4: The Hologenome - YouTube
Agriculture, Environment and the Developing World: A Future of PCR. Part 4: The Hologenome Plenary lecture by Richard Jefferson, CEO Cambia, Cold Spring Harbor, September, 1994. 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, integral to the complex system in which it lives. This implied 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 impacting hormone action informed this hypothesis. References was made to work indicating that mating pheromones were only released after skin microbiota activated the precursors.
At the 14th South African Congress of Biochemistry and Molecular Biology in 1997, Jefferson described how the modulation of steroid and other hormone levels by microbial glucuronidases and arylsulfatase profoundly impacted the performance of the composite entity. Following on work done isolating numerous and diverse glucuronidases from microbial samples of African animal feces, and their differential cleavage of hormones, he hypothesized that this phenomenon, microbially-mediated hormone modulation, could underlie evolution of disease and social behavior as well as the holobiont fitness and system resilience. In his lectures, Jefferson coined and defined the term 'Ecotherapeutics', referring to adjustment of the population structure of the microbial composition in plants and animals - the microbiome - and their support ecosystem to improve performance. In 2007, Jefferson followed with a series of posts on the logic of hologenome theory on Cambia's Science as Social Enterprise page.
In 2008, Eugene Rosenberg and Ilana Zilber-Rosenberg apparently independently used the term hologenome and developed the hologenome theory of evolution. This theory was originally based on their observations of Vibrio shiloi-mediated bleaching of the coral Oculina patagonica. Since its first introduction, the theory has been promoted as a fusion of Lamarckism and Darwinism and expanded to all of evolution, not just that of corals. The history of the development of the hologenome theory and the logic undergirding its development was the focus of a cover article by Carrie Arnold in New Scientist in January, 2013."Creator of Species, The Hologenome, a New View of Evolution" https://www.newscientist.com/article/mg21728992-000-the-hologenome-a-new-view-of-evolution/ A comprehensive treatment of the theory, including updates by the Rosenbergs on neutrality, pathogenesis and multi-level selection, can be found in their 2013 book."The Hologenome Concept: Human, Animal and Plant Microbiota"
In 2013, Robert Brucker and Seth Bordenstein re-invigorated the hologenome concept by showing that the gut microbiomes of closely related Nasonia wasp species are distinguishable, and contribute to hybrid death. This set interactions between hosts and microbes in a conceptual continuum with interactions between genes in the same genome. In 2015, Bordenstein and Kevin R. Theis outlined a conceptual framework that aligns with pre-existing theories in biology.
Support from vertebrate biology Multicellular life is made possible by the coordination of physically and temporally distinct processes, most prominently through hormones. Hormones mediate critical activities in vertebrates, including ontogeny, somatic and reproductive physiology, sexual development, performance and behaviour.
Many of these hormones – including most steroids and thyroxines – are secreted in inactive form through the endocrine and apocrine systems into epithelial corridors in which microbiota are widespread and diverse, including gut, urinary tract, lung and skin. There, the inactive hormones can be re-activated by cleavage of the glucuronide or sulfate residue, allowing them to be reabsorbed. Thus the concentration and bioavailability of many of the hormones is impacted by microbial cleavage of conjugated intermediaries, itself determined by a diverse population with redundant enzymatic capabilities. Aspects of enterohepatic circulation have been known for decades, but had been viewed as an ancillary effect of detoxification and excretion of metabolites and xenobiotics, including effects on lifetimes of pharmaceuticals, including birth control formulations.
The basic premise of Jefferson's first exposition of the hologenome theory is that a spectrum of hormones can be re-activated and resorbed from epithelia, potentially modulating effective time and dose relationships of many vertebrate hormones. The ability to alter and modulate, amplify and suppress, disseminate and recruit new capabilities as microbially-encoded 'traits' means that sampling, sensing and responding to the environment become intrinsic features and emergent capabilities of the holobiont, with mechanisms that can provide rapid, sensitive, nuanced and persistent performance changes.
Studies by Froebe et al. in 1990 indicating that essential mating pheromones, including androstenols, required activation by skin-associated microbial glucuronidases and sulfatases. In the absence of microbial populations in the skin, no detectable aromatic pheromone was released, as the pro-pheromone remained water-soluble and non-volatile. This effectively meant that the microbes in the skin were essential to produce a mating signal.Enabling Innovation: A 2011 Lecture in the Illahee Series https://vimeo.com/26387884
Support from coral biology Subsequent re-articulation describing the hologenome theory by Rosenberg and Zilber-Rosenberg, published 13 years after Jefferson's definition of the theory, was based on their observations of corals, and the coral probiotic hypothesis.
Coral reefs are the largest structures created by living organisms, and contain abundant and highly complex microbial communities. A coral "head" is a colony of genetically identical polyps, which secrete an exoskeleton near the base. Depending on the species, the exoskeleton may be hard, based on calcium carbonate, or soft and proteinaceous. Over many generations, the colony creates a large skeleton that is characteristic of the species. Diverse forms of life take up residence in a coral colony, including photosynthetic algae such as Symbiodinium, as well as a wide range of bacteria including nitrogen fixers, and chitin decomposers, all of which form an important part of coral nutrition. The association between coral and its microbiota is species dependent, and different bacterial populations are found in mucus, skeleton and tissue from the same coral fragment.
Over the past several decades, major declines in coral populations have occurred. Climate change, water pollution and overfishing are three stress factors that have been described as leading to disease susceptibility. Over twenty different coral diseases have been described, but of these, only a handful have had their causative agents isolated and characterized.
Coral bleaching is the most serious of these diseases. In the Mediterranean Sea, the bleaching of Oculina patagonica was first described in 1994 and, through a rigorous application of Koch's Postulates, determined to be due to infection by Vibrio shiloi. From 1994 to 2002, bacterial bleaching of O. patagonica occurred every summer in the eastern Mediterranean. Surprisingly, however, after 2003, O. patagonica in the eastern Mediterranean has been resistant to V. shiloi infection, although other diseases still cause bleaching.
The surprise stems from the knowledge that corals are long lived, with lifespans on the order of decades, and do not have adaptive immune systems. Their innate immune systems do not produce antibodies, and they should seemingly not be able to respond to new challenges except over evolutionary time scales. Yet multiple researchers have documented variations in bleaching susceptibility that may be termed 'experience-mediated tolerance'. The puzzle of how corals managed to acquire resistance to a specific pathogen led Eugene Rosenberg and Ilana Zilber-Rosenberg to propose the Coral Probiotic Hypothesis. This hypothesis proposes that a dynamic relationship exists between corals and their symbiotic microbial communities. Beneficial mutations can arise and spread among the symbiotic microbes much faster than in the host corals. By altering its microbial composition, the "holobiont" can adapt to changing environmental conditions far more rapidly than by genetic mutation and selection in the host species alone.
Extrapolating the coral probiotic hypothesis to other organisms, including higher plants and animals, led to the Rosenberg's support for and publications around the hologenome theory of evolution.
Theory
Definition
The framework of the hologenome theory of evolution is as follows (condensed from Rosenberg et al., 2007): "All animals and plants establish symbiotic relationships with microorganisms." "Different host species contain different symbiont populations and individuals of the same species can also contain different symbiont populations." "The association between a host organism and its microbial community affect both the host and its microbiota." "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."