My personal thoughts on Bordenstein & Theis Holobiont Paper – part 3 – terminology

Continuing on from The Tree of Life: My personal thoughts on Bordenstein and Theis Holobiont Paper – part 2 and The Tree of Life: My personal thoughts on Bordenstein and Theis: Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes

I am going to skip over the main Box 1 for now.  And go to Box 2 – Terminology because this will be important for the rest of the article

Box 2. Terminology

Coevolution: reciprocal evolution of interacting species

Seems OK.

Commensalism: a relationship benefiting one party while the other is unaffected

I am good with this.  Though I do wonder if they mean that this is a form of symbiosis or if it applies to any interaction even one that is not a symbiosis.  When I teach this I treat commensalism as a form of symbiosis.

Mutualism: a relationship benefiting both parties

Same comment as for commensalism

Parasitism: a relationship benefiting one party to the other’s detriment

Same comment as for commensalism and mutualism.

Symbiosis: two or more species living closely together in a long-term relationship

I am good with this

Macrobe: a eukaryotic host, most being visible by eye

I don’t think I like this.  Why does a macrobe have to be a eukaryote?

Microbiota: the microbes in or on a host, including bacteria, archaea, viruses, protists, and fungi

I am ok with this.  Though it would have been helpful to define host.

Microbiome: the complete genetic content of the microbiota

I do not like this use of microbiome personally.   See more here: What does the term microbiome mean? And where did it come from? A bit of a surprise ..

Holobiont: a unit of biological organization composed of a host and its microbiota

I am OK with this if the authors what to use it as a proposed definition to then test.  However, I am not at this point convinced that a there is a “unit” of biological organization here.  I would I guess prefer a holobiont to be defined as a “host and its microbiota” without the “unit of biological organization part”

Hologenome: the complete genetic content of the host genome, its organelles’ genomes, and its microbiome

I am OK with this as a proposed definition.

Microbe flow: the exchange of microbes between holobionts

Seems OK.

Phylosymbiosis: microbial community relationships changing in parallel with the host nuclear phylogeny

This seems potentially very useful to distinguish something from co-evolution.

Hologenome Concept of Evolution
The hologenome concept of evolution was first explicitly introduced in 1994 during a symposium lecture by Richard Jefferson [56], and it was independently derived in 2007 by Eugene Rosenberg and Ilana Zilber-Rosenberg [57]. 

Good to see some of the history here. And since Richard Jefferson has been talking to me about this for many years it is good to see him mentioned.

It posits that hosts and their microbiota are emergent individuals, or holobionts, that exhibit synergistic phenotypes that are subject to evolutionary forces [35–37]. 

I am fine with this as a “posit”.  Not saying I agree it is true.  But here it is presented clearly as what the Hologenome Concept implies.

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. 

OK again as an explanation of the model.

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 [35–37,58]. 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 [58]. 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.

I am fine with all of this as an explanation of the model / concept.  Again, not saying I think it is right but good to see it laid out pretty clearly.

Author: Jonathan Eisen

I am an evolutionary biologist and a Professor at U. C. Davis. (see my lab site here). My research focuses on the origin of novelty (how new processes and functions originate). To study this I focus on sequencing and analyzing genomes of organisms, especially microbes and using phylogenomic analysis View all posts by Jonathan Eisen