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) 
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 .
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 .
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.
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 .
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.
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.
13 thoughts on “My personal thoughts on Bordenstein and Theis Holobiont Paper – part 2”
Generally good summary and appreciate thoughts. Only concern is that you might be over sensitive to tone when intent of essay is to be provocative. PLoS essays supposed to be “opinionated articles” with an “imaginative approach to a provocative question”. Just the rules. Let's embrace that format. We've solicited feedback from 15 colleagues before publishing the article. No one adversely reacted to the tone and appreciated the unique format. Some didn't even think it was provocative but rather a review. It's somewhere in the middle IMO.
Hi Jonathan, for additional reading by others on centrality of microbes & what is a host, recommend the following articles. Of course, there are many out there. But the point is that these ideas are coming from the community, not just one article.
Giving microbes their due: http://www.ncbi.nlm.nih.gov/pubmed/26085673
What is a host?: http://iai.asm.org/content/early/2014/11/05/IAI.02627-14.full.pdf+html
Animals in a bacterial world: http://www.ncbi.nlm.nih.gov/pubmed/23391737
Re “Only concern is that you might be over sensitive to tone when intent of essay is to be provocative. PLoS essays supposed to be “opinionated articles” with an “imaginative approach to a provocative question”. Just the rules. Let's embrace that format. “
Well, I honestly don't embrace the format in the way you want me to. Here are some comments about this:
1. Editors of journals ask for all sorts of things but in the end what is in a paper is the responsibility of the authors.
2. I am not privy to the communications you had with the editors. Nor are the readers of this article.
3. If you look at your article nowhere does it say “This is meant to be provacative”. If one clicks on the link near the top, and reads the guidance for authors of essays it does mention the “Essays take an imaginative approach to a provocative question” you mention above. But when people read this as a PDF, or in Pubmed Central or elsewhere how are they to know what your instructions were?
4. I note – the description of Essays by PLOS Biology does not say to be provacative. It says to “Essays take an imaginative approach to a provocative question”. Actually pretty different to me than “intent of essay is to be provocative”
5. The Essay description also says “engaging though rigorous investigation of the problem” and many of my concerns are that the wording is not as rigorous as I would like. One can be provacative and also rigorious by making clear when something is an opinion and when something is a supposed statement of fact or consensus. And I honestly do not think you did a good job of this in some sections. I am concerned that when people read this they will take many of the things you have written as being accepted by the community or as facts when I disagree. And I believe it is valid to point this out.
“3. If you look at your article nowhere does it say “This is meant to be provacative”. If one clicks on the link near the top, and reads the guidance for authors of essays it does mention the “Essays take an imaginative approach to a provocative question” you mention above. But when people read this as a PDF, or in Pubmed Central or elsewhere how are they to know what your instructions were?”
Why do you underestimate the IQ of the readers? Do people really need some instructions to recognize a novel, provocative and, I daresay, visionary paper?
“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?”
Why is “nearly” a problem? Anyway, if Bordenstein's paper makes some scientists to consider certain phenomena previously taken for granted, and research a potential, previously unexplored role of microbes in say, xylem formation, the better!
Reading this paper makes me thinking: what is a host? What is a guest? Is it a guest? What is hologenome here?
“An Endophyte Constructs Fungicide-Containing Extracellular Barriers for Its Host Plant” (2015)
Some fiar points. But I note – if you go back to the beginning. Seth expressed concern that some people had not read his paper. So I decided to actually read it, line for line, and say what I thought. And I think many of the statements here misrepresent the current state of knowledge of the field.
Note – annoying that Blogger does not simply make links out of web addresses but you can use html in the comments to turn them into links.
Giving microbes their due
What is a host?
Animals in a bacterial world
Im thrilled that we have a stimulated area around the hologenome. The new plos article claims it is relevant (read last sentence or two), though it does curiously send mixed messages.
Jonathan – u did quickly take my comment of out of context. Here it is from Symbionticism blog – rather easy to see why I said that. If they were sloppy about this, what else should we question about _their_ analysis?
“From the start in paragraph 2, it wasn't clear if M&S read our publication in detail. They attribute the origin of the word “holobiont” to Mindell (1992) but we showed that it was first used by Lynn Margulis in 1991. I had the pleasure of corresponding with Mindell prior to our publication, and he humbly tipped us off to the false credit.
As we state…
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. Amid the flourishing of host microbiome studies, holobiont is now generally used to mean every macrobe and its numerous microbial associates [19,22]”
I also clarified this to you on twitter.
Gemma, thank you for the kind and generous comments about the paper. Im glad you read it this way too.
As a microbiome community, we should be laser focussed on speaking the same language and definitions (this is not happening in published critique of hologenome), and avoid the similar kerfuffle over what is a pathogen? We are in the advantageous spot of being early in the discipline where words like holobiont and hologenome could become useful to many.
Seth – I was not critiquing your claim about people not reading your paper. I listened to you. And, I note, I had not read the paper exceptionally carefully either. So I thought I would read it. But of course, since I am into sharing, I thought, why not, in essence, read it publicly and comment along the way.
“And I think many of the statements here misrepresent the current state of knowledge of the field.”
Let's be precise. The statements in the paper represent a novel model/concept. Though YOUR current state of knowledge of the field(s) may not be sufficient to comprehend, or integrate them.
Do not misunderstand, please. This is absolutely not against you. The last polymath died in 1519.
I fundamentally disagree with your assessment here. The paper is presenting both theories and then claiming their is evidence for those theories. I think in sections they do a poor job of distinguishing between the two. And when they make claims about the state of knowledge in the field that are inaccurate this should be questioned especially as it is being used to support their models.
When sections are clear about what is a theory and what is a fact those sections are fine. And useful. But I believe in many sections they either mix the two up (without making it clear) or get the state of the field wrong.
And it is important when discussing novel ideas to not get confused as to what is unsubstantiated theory and what is generally accepted.
You are welcome. My personal opinion is that your paper is visionary, and should hopefully open many eyes.
“…and avoid the similar kerfuffle over what is a pathogen?”
Absolutely. The endophytic fungi in the plants are a nice example. Mutualists, commensals, symbionts or pathogens? It depends. The borders are fuzzy indeed, lifestyle switching is a norm.
“And it is important when discussing novel ideas to not get confused as to what is unsubstantiated theory and what is generally accepted.”
I understand your points. But “generally accepted” does not necessarily mean right and correct.
Re “. But “generally accepted” does not necessarily mean right and correct.”
Yes, agreed 100%