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.

My personal thoughts on Bordenstein and Theis Holobiont Paper – part 2

See this The Tree of Life: My personal thoughts on Bordenstein and Theis: Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes for part 1 and background.  I note – part of why I wrote the previous post was Seth had complained in a blog post that some authors seemed to have not read his paper.  So I decided to read it.  And to comment on it publically.

After I posted about this there was some back and forth with Seth on Twitter.  Here is some of it:

Anyway, I am going through, sentence by sentence the paper.

I did the Abstract in the last post.  Now on to the Introduction

“The time has come to replace the purely reductionist ‘eyes-down’ molecular perspective with a new and genuinely holistic, eyes-up, view of the living world, one whose primary focus is on evolution, emergence, and biology’s innate complexity.”—Carl Woese (2004) [1]

Nice quote.

At the end of the 19th century, the theory of evolution via natural selection was birthed with the appreciation that individual animals and plants vary in their phenotypes and that competition at the individual level drives gradual change in the frequencies of these phenotypes [2]. 

No comments.

From this early vantage point, fusing evolution with Mendelian genetics in the early 20th century was a seamless transition in biology, namely one based on the framework that phenotypes in the individual animal and plant are encoded by the nuclear genome under the laws of Mendelian inheritance [3–5].

I really do not feel comfortable calling this a seamless transition.  From my reading and what I know of the history, it took a lot of work by people to both figure out how to make this transition, how to refine it and then how to convince others that it was correct.

In the mid-20th century, the modern synthesis grounded the nucleocentric foundation of zoology and botany in three areas: (1) the nuclear mutability and recombinogenic nature of organisms, (2) the sorting of this genetic variation by natural selection, and (3) the observations that macroevolutionary processes such as the origin of species can be explained in a manner that aligns with Mendelian genetics and microevolutionary mechanisms [6].

Calling zoology and botany “nucleocentric” seems unnecessary to me although I guess I am not sure what they point of this is.

The foundation of the modern synthesis remains as scientifically sound today as when it was conceived. 

I am not sure I understand what this is saying.  How would the scientific soundness of the synthesis change over time?  Or do they mean here “the perception of the scientific soundness?”

However, it is critical to recognize that microbiology was largely divorced from these early epochs in the life sciences.

Agreed.

The modern synthesis commenced at a time when the germ theory of disease dictated the prevailing wisdom on microbes, and the molecular tools used to understand the microbial world and its influence were inferior to those available now [7–11].

This is true but the tools were also inferior for characterizing anything.  Plus I do not think it was the molecular tools per se that changed things.  It was also ideas and theories.

The theories of gradual evolution and the modern synthesis were thus forged during periods of eukaryocentricism and nucleocentrism that did not appreciate the centrality of microbiology in zoology and botany because of limitations in perspective and technology.

Yes, good to mention the “limitations in perspective”.  But I am not sure what eukaryocentrism is exactly.  Or what nucleocentrism is either.  And I just do not feel comfortable with the “centrality of microbiology in zoology and botany statement”.  This seems to be putting the cart before the horse.  Are they central?  I don’t actual know.  Are they important?  Absolutely.  That is why I study host-microbe interactions.  But are they “central” – I would not go that far.  And I thought part of the point of this was that we need to test that, not posit it.

Today, there is an unmistakable transformation happening in the way that life is comprehended [12–16], and it is as significant for many biologists as the modern synthesis. Animals and plants are no longer viewed as autonomous entities, but rather as “holobionts” [17–21], composed of the host plus all of its symbiotic microbes (definitions in Box 1). 

I find this to be an enormous overstatement.  I for one do not believe we are even remotely near a point where understanding that plants and animals are “not autonomous entities” is getting to something akin to the modern synthesis.

The term “holobiont” traces back to Lynn Margulis and refers to symbiotic associations throughout a significant portion of an organism’s lifetime, with the prefix holo- derived from the Greek word holos, meaning whole or entire. 

I was not aware of the history.

Amid the flourishing of host microbiome studies, holobiont is now generally used to mean every macrobe and its numerous microbial associates [19,22], and the term importantly fills the gap in what to call such assemblages. 

I am not so sure that this is a useful term and I am not convinced that it “importantly” fills any gap.  Whether it fills any gap depends entirely on whether many of the claims in this paper are supported by evidence.  So stating this in the introduction seems awkward.

Symbiotic microbes are fundamental to nearly every aspect of host form, function, and fitness, including in traits that once seemed intangible to microbiology: behavior [23–26], sociality [27–30], and the origin of species [31]. 

I agree that microbes play more of a role than was thought.  I don’t think they play fundamental roles in “nearly every aspect of host form, function and fitness.”  What about vision? Xylem formation? Meiosis? Speech? Muscle contraction? Flight mechanics? And 100,000 other things.  Sure, microbes play fundamental roles in many aspects of host biology.  And that is awesome and why I study host-microbe interactions.  But this “nearly every aspect” is just really way overboard.

The conviction for a central role of microbiology in the life sciences has been growing exponentially, and microbial symbiosis is advancing from a subdiscipline to a central branch of knowledge in the life sciences [14,32–35].

I don’t find this convincing.

This revelation brings forth several newly appreciated facets of the life sciences, including the testable derivation that the nuclear genome, organelles, and microbiome of holobionts comprise a hologenome [35–37]. 

Ok.  This I am OK with.  Because rather than overstating things this presents something, finally, as something to test.

The hologenome concept is a holistic view of genetics in which animals and plants are polygenomic entities. Thus, variation in the hologenome can lead to variation in phenotypes upon which natural selection or genetic drift can operate. 

This seems to be presenting material as fact rather than hypothesis.

While there is a rich literature on coevolutionary genomics of binary host–microbe interactions, there have been few systematic attempts to align the true complexity of the total microbiome with the modern synthesis in a way that integrates these disparate fields [38–40].

I generally agree with this.

The object of this essay is to make the holobiont and hologenome concepts widely known. We clarify and append what they are and are not, explain how they are both consistent with and extend existing theory in ecology and evolutionary biology, and provide a predictive framework for evaluating them.

OK.

Our goal is to provide the main conceptual foundation for future hypothesis-driven research that unifies perceived divisions among subdisciplines of biology (e.g., zoology, botany, and microbiology) and advances the postmodern synthesis that we are now experiencing [41,42]. 

This rubs me the wrong way.  To aim to “provide the main conceptual foundation” seems to be exceptionally bold and arrogant.  And to, in this one paper provide such a conceptual foundation – I don’t think so.  And then to advance the post modern synthesis too?  How about we judge that AFTER the article is published not before?

We distill this topic with evidence-based reasoning to present the ten principles of holobionts and hologenomes (summarized in Box 1).

I guess I don’t really like this either.  “The” 10 principles?  How about just “10 principles”.  As this is written it implies there are no other principles that could be hypothesized.

OK … so that is the Introduction.  Will try to continue with the meat of the paper soon.

UPDATE: See part 3 here.

My personal thoughts on Bordenstein and Theis: Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.

There are many discussions going on about a paper from Bordenstein and Theis that was published in PLOS Biology in August 2015. The paper is Bordenstein SR, Theis KR (2015) Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes. PLoS Biol 13(8): e1002226. doi:10.1371/journal.pbio.1002226

A few days ago a paper came out by Moran and Sloan that discussed an alternative view of Hologenomes: Moran NA, Sloan DB (2015) The Hologenome Concept: Helpful or Hollow? PLoS Biol 13(12): e1002311. doi:10.1371/journal.pbio.1002311.

I made some comments on Twitter when the 1st paper came out about how I was skeptical of the paper and in discussions with Seth Bordenstein I said I would try to write up my thoughts.  And when I was pointed to the second paper today I posted to Twitter that I thought it was important and got into a brief discussion with Seth about the paper. 
In thinking about the papers and science publishing and scientific discussions I have decicded to try and carry out a new experiment.  I am going to go, as fast as I can, line for line through the papers and post my thoughts in response to those lines.  And I will try to be honest even if my thoughts are not, well thought out or nice or helpful.  I am just going to post the thoughts.  And one reason I want to do this is I worry (or maybe realize) that my judgement may be being affected here by visceral responses to some of the lines.  In particular, I confess, some of the way the Bordenstein and Theis article is written really rubs me the wrong way.  Nothing personal against the authors.  But the text did not agree with me in parts.  And I think that may have affected my response to the article.  I do not know for sure but it seems possible.  
Regardless, I am going to try and go through this.  And for now I am going to just start with the Abstract.

Groundbreaking research on the universality and diversity of microorganisms is now challenging the life sciences to upgrade fundamental theories that once seemed untouchable.

I personally find this to be a bit too extreme. Really – did they once seem untouchable? To whom?

To fully appreciate the change that the field is now undergoing, one has to place the epochs and foundational principles of Darwin, Mendel, and the modern synthesis in light of the current advances that are enabling a new vision for the central importance of microbiology.  

I think it is overstating the “central importance of microbiology” to place it somehow in line with Darwin, Mendel and the modern synthesis

Animals and plants are no longer heralded as autonomous entities but rather as biomolecular networks composed of the host plus its associated microbes, i.e., “holobionts.” 

While on the one hand I agree with part of this statement I think it is making a claim and stating it as a fact when this is what is being debated.

 As such, their collective genomes forge a “hologenome,” and models of animal and plant biology that do not account for these intergenomic associations are incomplete. 

Certainly animal and plant biology has to account for microbes. But it is false logic to say that one can only account for microbes by following the hologenome concepts.

Here, we integrate these concepts into historical and contemporary visions of biology and summarize a predictive and refutable framework for their evaluation. 

No thoughts on this.

Specifically, we present ten principles that clarify and append what these concepts are and are not, explain how they both support and extend existing theory in the life sciences, and discuss their potential ramifications for the multifaceted approaches of zoology and botany. 

Confession. Saying ones own principles “clarify” something rubs me the wrong way. I would really have preferred it if they said “attempt to clarify”.

We anticipate that the conceptual and evidence-based foundation provided in this essay will serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology’s subdisciplines. 

I find this to be really overstated too. I don’t think what you have presented in this paper is a roadmap. And for you to call it that sets up this essay as basically saying that everything else that has come before is limited and lame.

At a time when symbiotic microbes are recognized as fundamental to all aspects of animal and plant biology, the holobiont and hologenome concepts afford a holistic view of biological complexity that is consistent with the generally reductionist approaches of biology. 

I do not think symbiotic microbes are fundamental to all aspects of animal and plant biology. I think this is actually a silly statement and makes me doubt the objectivity of the authors.

  UPDATE: See part 2 here.