ARTICLE: “Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.”
Bordenstein SR, Theis KR (2015) “Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.” PLoS Biol 13(8): e1002226.
FULL TEXT:
https://doi.org/10.1371/journal.pbio.1002226
THE 10 PRINCIPLES OF HOLOBIONTS AND HOLOGENOMES:
I. Holobionts and hologenomes are units of biological organization
Complex multicellular eukaryotes are not and have never been autonomous organisms, but rather are biological units organized from numerous microbial symbionts and their genomes.
Biomolecular associations between host and microbiota are more conceptually similar to an intergenomic, genotype x genotype interaction than a genotype x environment interaction.
II. Holobionts and hologenomes are not organ systems, superorganisms, or metagenomes
As holobionts are complex assemblages of organisms consisting of diverse microbial genomes, biology should draw a clear distinction between holobionts/hologenomes and other terms that were not intended to describe host–symbiont associations.
Organ systems and superorganisms are biological entities comprised of one organism’s genome; metagenome means “after” or “beyond” the genome, does not intrinsically imply organismality, and obviates the fundamentals of symbiosis in the holobiont.
III. The hologenome is a comprehensive gene system
The hologenome consists of the nuclear genome, organelles, and microbiome.
Beneficial, deleterious, and neutral mutations in any of these genomic subunits underlie hologenomic variation.
IV. The hologenome concept reboots elements of Lamarckian evolution
Although Lamarck never imagined microbes in his theory, applying the tenets to holobionts rebirths some major aspects of Lamarckism.
The nuclear genome is inherited mainly within a Mendelian framework, but the microbiome is originally acquired from the environment and may become inherited.
Host–microbe associations can forge disequilibria via parental transfer or stable environmental transmission.
V. Hologenomic variation integrates all mechanisms of mutation
Every hologenome is a multiple mutant, meaning that there is variation across many individual genomes spanning the nucleus, organelles, and microbiome.
Base pair mutation, horizontal gene transfer, recombination, gene loss and duplication, and microbial loss and amplification are all sources of variation.
VI. Hologenomic evolution is most easily understood by equating a gene in the nuclear genome to a microbe in the microbiome
Evolution for both genes and symbionts is fundamentally a change in population frequency over successive generations, i.e., the fraction of holobionts carrying that particular nuclear allele or microbe.
Covariance of hosts and microbes in a holobiont population (i.e., community genetics) follows a theoretical continuum directly to coinheritance of gene combinations within a genome (i.e., population genetics).
A grand unified theory of evolutionary and ecological genetics deserves priority attention.
VII. The hologenome concept fits squarely into genetics and accommodates multilevel selection theory
Multilevel selection theory asserts that selection operates across multiple levels of genetic variation with phenotypic effects, from genes to hologenomes and beyond.
Holobionts are exclusive to hosts and their associated microbiota; different holobionts, such as a pollinator and a flower, interact with each other under standard ecological principles.
VIII. The hologenome is shaped by selection and neutrality
Natural selection can work to remove deleterious nuclear mutations or microbes while spreading advantageous nuclear mutations or microbes; in the absence of selection, the neutral spread of hologenomic variation through populations is an inherently stochastic process.
Mixed ecological models of stochastic and deterministic community assembly likely reflect natural systems, and partitioning the microbiota into stochastic versus deterministic subunits will be an important future goal of the field.
IX. Hologenomic speciation blends genetics and symbiosis
The Biological Species Concept was never intended to be exclusive of symbiosis, though history largely divorced the two and created unnecessary controversy.
Antibiotic or axenic experiments in speciation studies must be a routine, if not obligatory, set of experiments in genetic analyses of speciation for an all-inclusive understanding of the origin of species.
X. Holobionts and their hologenomes do not change the rules of evolutionary biology
Although the concepts redefine that which constitutes an individual animal or plant, they are not a fundamental rewriting of Darwin’s and Wallace’s theory of evolutionary biology.
Simply put, if the microbiome is a major, if not dominant, component of the DNA of a holobiont, then microbiome variation can quite naturally lead to new adaptations and speciation, just like variation in nuclear genes.
Terminology
Coevolution: reciprocal evolution of interacting species
Commensalism: a relationship benefiting one party while the other is unaffected
Mutualism: a relationship benefiting both parties
Parasitism: a relationship benefiting one party to the other’s detriment
Symbiosis: two or more species living closely together in a long-term relationship
Macrobe: a eukaryotic host, most being visible by eye
Microbiota: the microbes in or on a host, including bacteria, archaea, viruses, protists, and fungi
Microbiome: the complete genetic content of the microbiota
Holobiont: a unit of biological organization composed of a host and its microbiota
Hologenome: the complete genetic content of the host genome, its organelles’ genomes, and its microbiome
Microbe flow: the exchange of microbes between holobionts
Phylosymbiosis: microbial community relationships changing in parallel with the host nuclear phylogeny
Hologenome Concept of Evolution
The hologenome concept of evolution was first explicitly introduced in 1994 during a symposium lecture by Richard Jefferson, and it was independently derived in 2007 by Eugene Rosenberg and Ilana Zilber-Rosenberg. It posits that hosts and their microbiota are emergent individuals, or holobionts, that exhibit synergistic phenotypes that are subject to evolutionary forces. Via fidelity of transmission from parents to offspring or stable acquisition of the microbiome from the environment, covariance between the host and microbiota can be established and maintained. Consequently, as with phenotypes encoded by nuclear genomes, phenotypes encoded by beneficial, deleterious, and neutral microbes in the microbiome are subject to selection and drift within holobiont populations. Genetic variation among hologenomes can arise through changes to host genomes as well as through changes to the genomes of constituent symbiotic microbes . The microbiomes, and thus their encoded phenotypes, can change through differences in the relative abundances of specific symbiotic microbes, the modification of the genomes of existing resident microbes, or the incorporation of new microbial symbionts into holobionts, which can occur even within the reproductive lifetime of hosts. Importantly, genetic variation in the microbiome vastly exceeds that in the host genome and accumulates much more rapidly than variation in host genomes. Therefore, given that genetic variation is the raw material upon which evolution ultimately acts, microbial sources of hologenomic variation are potential targets of evolution, and, despite its inherent complexity, biologists must consider the incorporation of the microbiome in the overall study of evolution.