Wednesday, December 09, 2015

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.


  1. Just adding my two cents Jonathan. Man-love for you, and I welcome the discussion. We've already corresponded a bit over twitter, but just placing a record here.

    First, I have laid out a critique of the new hologenome publication at my blog. There is a mixture of inaccurate and mixed arguments that I detail. We are now working on a formal response at PLOS:

    Second, I look forward to discussing the issues in depth with you in a collaborative Q&A format so that the community delves deeply into the biology rather than word-usage. Otherwise, we risk running into one-sided rants at our respective blogs. And a relevant note here. The PLOS essays format is by definition an "opinionated" format to drum up discussion of significant topics. We restrict this style to this format.

    Sincerely -Seth

    1. thanks Seth

      Note - I am not sure what you mean about the word-usage comment. I was reading your words of your essay and trying to interpret your words. I agree it would be good to have an open discussion about the biology but this is a published paper. And I think it is useful to look at what it says. If you meant something other than what you wrote, fine, but as this is out there I am going to try and go through it and read what it says.

    2. Fair enough. I don't know what I meant by word-usage either. Ill list a few thoughts now right off the top of my head to explain where Im coming from. We had over 15 colleagues read the paper - friends and skeptics. No one gave us this kind of feedback. We also solicited feedback from the community at large.

      1. Yes, the role of microbial communities in a number of fields has been mostly new to biologists in the last decade. There is nothing to be overly cautious about here. I know you know this too. We give examples in the text.

      2. It is very difficult to overstate the "centrality of microbiology" in biology these days. M&S note the revolution. Eugene Koonin has written extensively about this in addition to lectures by Margaret McFall-Ngai. For Koonin, see and

      3. Does anyone really doubt that hosts and portions of the microbial community are not talking to each other via metabolites, proteins, etc? This is the bimolecular network that is very much reality, not a debate. I know you know this.

      4. It is not false logic to claim that the genomes of host and members of the microbial community are producing products that interact, and that studying the biology of one may be only half of the story. This is essentially repeating my point three.

      5. NA

      6. Either is fine with me

      7. You prescribe intent of "limited and lame" that is wholly unjustified. And yes, it is a roadmap that boils the hologenome concept into ten simple principles and provides several examples of how to test some of them. This was sorely needed to mitigate confusion and provide an experimental framework rather than examples that support the hologenome concept.

      8. When tested carefully, what trait has not been affected by the microbiome? That's where this statement is coming from. But sure, we could have used "nearly" all aspects as we do in the text.

    3. Re: "When tested carefully, what trait has not been affected by the microbiome? "

      There is a big big big difference between saying microbes are "fundamental to all aspects of animal and plant biology" and "what trait has not been affected by the microbiome". I am with you that basically all aspects of animals and plant biology can be effected by the microbiome. But that does not make them fundamental. For example, microbiomes can affect vision because microbes can cloud the fluid around eyes. But that does not make them "fundamental" to vision unless you are using a very unusual definition of fundamental.

  2. Thrilled to continue this more collaboratively in a Q&A in a bit. Need to response to PLOS first before I can directly get back to this again.