Friday, June 12, 2015

What are Holobionts and Hologenomes?

Updated 08/09/16:

1. The article referred to below is now published at PLOS Biology (Bordenstein and Theis 2015)

2. Holobionts are defined as the host plus of all its microbial symbionts, including transient and stable members. The term was originally and briefly defined in 1991 by Lynn Margulis in the book Symbiosis as a Source of Evolutionary Innovation (link) as a "compound of recognizable bionts". Bionts = organisms. The bionts can be cooperative or competitive. Please see the aforementioned PLOS article for details.

3. Hologenomes are then defined as the genomes of the holobiont, i.e., the host and microbial genomes, and the pluralistic attributes of a holobiont scale directly to the hologenome (Theis et al, 2016, mSystems). The terms were first used by Richard Jefferson in 2004 (link) and independently by Eugene Rosenberg and Ilana Zilber-Rosenberg in 2007 (link).

June 12, 2015
For the past eight months, Kevin Theis and I have been working hard on an essay on holobionts and their hologenomes. These terms and concepts are well known to a small cadre of biologists, but otherwise are mired in confusion and misinterpretation in part because the literature in this area is diffuse and sparse. Our paper has now gone through a mostly transparent review, and in and outside of that process, we have received some excellent feedback from colleagues in the community. I'm particularly interested in scaling the feedback up and crowdsourcing the process through the comments section below. Some of these principles may not make sense to the reader because we have not yet put forth the entire manuscript (due to be published this year). Nonetheless, I hope that some of what's below resonates with readers to stir a lively discussion. Thanks in advance for your perusal and feedback if you can. This is a draft in progress that can only improve with your insights. 

I. Holobionts and hologenomes are units of biological organization

o   Complex multicellular eukaryotes are not and have never been autonomous organisms, but rather are biological units organized from numerous microbial symbionts and their genomes
o   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

o   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
o   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 for environmental samples, and obviates the obviates the fundamentals of symbiosis in the holobiont

III. The hologenome is a comprehensive gene system

o   The hologenome consists of the nuclear genome, organelles, and microbiome
o   Beneficial, deleterious, and neutral mutations in any of these genomic subunits underlie hologenomic variation

IV. Hologenomic evolution is most easily understood by equating a gene in the nuclear genome to a microbe in the microbiome

o   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.
o   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)
o   A grand unified theory of evolutionary and ecological genetics deserves priority attention

V. Hologenomic variation integrates all mechanisms of mutation

o   Every hologenome is a multiple mutant meaning that there is variation across many individual genomes spanning the nucleus, organelles, and members of microbiome
o   Base pair mutation, horizontal gene transfer, recombination, gene loss and duplication, and microbial loss and amplification are all sources of variation

VI. The hologenome concept reboots elements of Lamarckian evolution

o   Although Lamarck never imagined microbes in his theory, applying the tenets to holobionts rebirths some major aspects of Lamarckism
o   The nuclear genome is inherited mainly within a Mendelian framework, but the microbiome is originally acquired from the environment and may become inherited
o   Host-microbe associations can forge disequilibria via parental transfer or stable environmental transmission

VII. The hologenome concept fits squarely into genetics and accommodates multi-level selection theory

o   Multi-level selection theory asserts that selection operates across multiple levels of genetic variation with phenotypic effects, from genes to hologenomes and beyond
o   Holobionts are exclusive to hosts and their associated microbiota. Different holobionts, such as a pollinator and flower, interact with each other under standard ecological principles

VIII. The hologenome is shaped by selection and neutrality

o   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
o   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

o   The Biological Species Concept was never intended to be exclusive of symbiosis, though history largely divorced the two and created unnecessary controversy
o   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

o   There is no fundamental rewriting of Darwin's and Wallace's theory of evolutionary biology, though the concepts redefine that which constitutes an individual animal or plant

o   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

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