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.
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
