The hologenome theory of evolution

I’d like to share an email exchange I had some months ago with Eugene Rosenberg, one of the authors of some extremely interesting papers outlining the hologenome theory of evolution.   He and his wife, Ilana Zilber-Rosenberg apparently completely independently from me articulated the hologenome theory from their experiences in microbiology and nutrition, and coral microbiology in particular.

In 2009, I found some Rosenberg papers describing the hologenome theory from 2008 and 2009.  I was delighted at the clear and lucid writing and exposition, and that their observations leading to the hologenome concept came from such a different field to my own.

My  development of the hologenome theory in 1991-1994 came from two avenues of work I’d been pursuing for some years:

1)  vertebrate commensal microbes and their role in controlling critical hormones necessary for macro-organism fitness and

2) the role of endophytic and epiphytic microbes in plant performance in agriculture, including of course rhizobia and numerous other plant-associated bacteria.

There’s no reasonable chance that my talks would have influenced or even been known to the Rosenbergs.   And this is a wonderful thing.  I sense that really good and useful theories come when different experiences and different observations require an explanation and a common framework can be independently derived to provide it.  This is certainly the case here.   The Rosenbergs observations of complex coral ecosystems, informed by a lifetime of microbiology, led to their version of the hologenome theory which is virtually identical to mine.

So when I wrote to Eugene, I was a bit tentative.  Many scientists are self-centred and territorial, and view the world and themselves through a ‘me-first’ lens.   These all-too-familiar scientists would view my disclosure of prior development of the hologenome theory as either threatening or in some way presumptuous.  The response I received, however, was  full of the joyful openness that we seek and admire in fine science and in life.  The email shows scientific generosity of spirit that does Professor Rosenberg, and indeed the profession proud.

When preparing this reading list, I stumbled onto a very recent and exciting paper (first listed) in PNAS, which describes the mating choice modulation associated (causally?) with microbial population changes in the holobiont, which Eugene alluded to in the email.

Its really an interesting paper that shows how altered microbiomes can be correlated with altered mating choice.  This is resonant with my 2007 blog and earlier lectures about how vertebrate mating choice is affected by glucuronide and sulfate metabolism of pheromones by vertebrate skin microbiome constituents (interestingly found by scientists at Colgate Palmolive!).

I strongly recommend readers look at their work.

Commensal bacteria play a role in mating preference of Drosophila melanogaster.

Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E.’

Proc Natl Acad Sci U S A. 2010 Nov 1. [Epub ahead of print]PMID: 21041648 [PubMed - as supplied by publisher]Related citations

The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework.

Rosenberg E, Sharon G, Zilber-Rosenberg I.

Environ Microbiol. 2009 Dec;11(12):2959-62. Epub 2009 Jun 30.PMID: 19573132 [PubMed - indexed for MEDLINE]Related citations

Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution.

Zilber-Rosenberg I, Rosenberg E.

FEMS Microbiol Rev. 2008 Aug;32(5):723-35. Epub 2008 Jun 28. Review.PMID: 18549407 [PubMed - indexed for MEDLINE]Related citatio

Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I.

Nat Rev Microbiol. 2007 May;5(5):355-62. Epub 2007 Mar 26. Review.PMID: 17384666 [PubMed - indexed for MEDLINE]

http://www.ncbi.nlm.nih.gov/pubmed

Email thread:

from: Eugene Rosenberg <eros@post.tau.ac.il>

to: Richard Jefferson <raj@cambia.org>

date: Wed, Mar 10, 2010 at 7:25 PM

subject: Re: Hologenome theory, microbiome / holobiont

Dear Richard,

Wow. What a joy to read your e-mail and blog. Before commenting, let me inform you that I am a young 75 year old general microbiologist that has published 250 scientific articles, almost exclusively on experimental studies on myxobacteria, hydrocarbon degradation by bacteria and more recently bacterial diseases of corals. My wife, Ilana, is the best nutritionist in Israel, with a strong background in biochemistry and microbiology. We came to the concept of the hologenome (I now include you in the “we”) from am attempt to explain how a particular coral became resistant to bacterial bleaching. Clearly, we share your view of the holobiont as a unit of selection in evolution of animals and plants.

Where do we go from here? Your clear discription of the glucuronide conjugate system is a fine example of how the microbes are an integral part of host metabolism. Furthermore you speculate that these reactions can lead to mating selection. Now to blow your mind- We have been working on the role of bacteria in mating selection for the last two years. It started when my wife found a paper in Evolution, published 20 years ago by Diane Dodd. She took a population of Drosophila from Bruce Canyon and raised half of them on a starch diet and the other half on maltose. After a year, she mixed them, and found the “starch flies” perfered to mate with ”starch flies” and “maltose flies” perfered to mate with “maltose flies.” Although they offered no explaination for this mating selection, my wife and I immediately thought bacteria. So, I put a graduate student, Gil Sharon, on the problem. He first repeated Dodd’s experiment using the standard laboratory strain of D. malanogaster and sucrose instead of maltose. Mating selection occurred after two generations and was maintained for 30 generations. When we added antibiotics, mating selection was abolished, indicating bacteria were responsible. Furthermore, we infected the antibiotic-treated flies with their homologous bacteria (isolated prior to antibiotic treatment) and mating selection was reestablished. We sent a manuscript to Nature and they rejected it, saying they would reconsider if we identified the specific bacterium responsible for the mating selection. This has not been an easy task, but we are still working on it.

Regardless of the particular bacterium, what is the mechanism? We have been extracting flies with pentane and doing GC-MS. There are differences between the “starch flies” and the “sucrose flies”.

Maybe the glucuronide system is involved.

It was a pleasure to hear from you. Let’s keep in contact.

Shalom

Eugene

Eugene Rosenberg, Professor Emeritus
Dept. of Molecular Microbiology and Biotechnology
Tel Aviv University
eros@post.tau.ac.il
+972-3-6409838

—– Original Message —–

From: Richard Jefferson

To: eros@post.tau.ac.il

Sent: Wednesday, March 10, 2010 8:27 AM

Subject: Hologenome theory, microbiome / holobiont relationships etc

Dear Professor Rosenberg,

I am writing firstly to compliment you and Professor Zilber-Rosenberg on your clear, lucid and compelling writing in the last years on the hologenome theory.

I have read these with great interest and pleasure.  I particularly commend you for the fine exposition in the FEMS and the Environmental Microbiology review and opinion piece, respectively.

I am a molecular biologist, and now as well innovation system strategist, currently with funding from the Gates Foundation.    I started work in molecular biology in 1974, and in the late 70′s and subsequently I began working with the glucuronide metabolism pathways of commensal vertebrate microbes, including E. coli.   It became very clear to me fairly early that the suite of capabilities to import, metabolize and ‘share’ the products of xenobiotic and endobiotic metabolism by gut microbes was central to the selective performance of the host and microbiome – the holobiont.

As I became involved in the earliest days of agricultural biotechnology, my focus on systems-level understanding and intervention continued to be informed by this awareness.   I was convinced that the model system approaches which were and are so joyously productive, may not have been as joyously instructive as to the workings and logic of natural systems as embedded through natural (or in agriculture, human) selection.

I’ve written about this approach a little, but I’m not very prolific as a writer (I would make a terrible academic, alas).  I have however been speaking and promoting this work for many years as part of my work as founder of Cambia – an international non-profit institution.

I attach to this a link to my blog (rarely visited, rarely updated) in which I wrote down some of my thoughts.  ( http://blogs.cambia.org/raj/index.php/2007/09/06/the-hologenome-hologenomics/ ).  I also have in my blog (the top of the blog) links to videos of lectures I”ve given at Cold Spring Harbor in 1994 on the hologenome, and its implications; and presentations in South Africa in 1997 (I’d love to share with you my old powerpoint if you’re interested) in which I refer to our molecular work on glucuronide metabolism and the logic of applying eco-therapeutics and the understanding and adjustment of the hologenome to health challenges.     Term ‘hologenome’ and ‘holobiont’ and its critical role in evolution were proposed by me at that CSH lecture and since, and I was overjoyed to read your parallel and independent articulation of their importance, especially with regard to the critical horizontal inheritance opportunities for the fitness of the selected holobiont in a complex environment.

This has continued to be my intellectual focus for much of the last 30 years, but most of my work has been focused on democratizing science-enabled innovation through ‘open source’ type approaches, and through increasing the transparency and fairness of intellectual property systems.

I would be thrilled to be in correspondence with you about these ideas – they shape my thinking in many fields, and I’m musing very hard about setting up experimental systems to test the hologenome theory, which to me is compelling.  My laboratory has been in storage now for over a year since our institute moved from Canberra to Brisbane, but within a year I expect I may be back to full steam.  I’ll likely be doing a ‘sabbatic’ of sorts at Berkeley  from July – December and look forward to getting back into the game, as our Initiative for Open Innovation goes to scale and can be taken over by other champions.

Again, my warmest wishes and congratulations for some of the best science writing I’ve read in a long time.  That we have arrived at virtually identical conclusions from such different perspectives is itself most gratifying.

Best wishes

Richard

Richard A. Jefferson PhD
Chief Executive Officer, Cambia
Director, Initiative for Open Innovation (IOI)
Professor of Science, Technology & Law
Queensland University of Technology (QUT)
G301, 2 George St, Brisbane 4000, QLD Australia
+61 419 499 753 (mobile)  +61 7 3138 4419 (work) +61 7 3138 4405 (fax)
www.bios.netwww.cambia.orgwww.patentlens.net  | www.openinnovation.org
e: r.jefferson@cambia.org

3 Responses

  1. Alexander SAVINOV says:

    Proc. IV Congress Rus. Soc. Parasitol. – RAS.
    «Parasitology in XXI century – problems, methods, solutions».
    Vol. 3. St. Petersburg: «Lema». 2008. P. 122–126

    AUTOCENOSIS AND DEMOCENOSIS – NEW CATEGORY FOR PARASITOLOGY, ECOLOGY AND EVOLUTIONARY BIOLOGY

    Savinov A.B.

    Nizhni Novgorod State University, pr. Gagarina 23-1,
    Nizhni Novgorod 603950 Russia,
    sabcor@mail.ru

    Abstract
    Representation about the population concerning a grouping bionts only one species version became classical. However achievements of modern ecology testify to it for organisms of various regular groups various symbolical attitudes (parasitism, mutualism), mentioning is a lot of levels of the organization (from subcellular up to organismic). Therefore on the basis of modern data about symbiogenesis (in various groups of organisms) and cybernetic positions the new paradigm is offered by the author according to whom everyone biont is formulated autocenosis, and the population – democenosis. In the synthetic theory of evolution elements of a population are bionts (organisms), and the population is presented by elementary evolutionary unit. From positions of the author as elementary evolutionary unit it should be considered democenosis. New categories «autocenosis» and «democenosis» should change gradually character of scientific thinking in ecology, parasitology and evolutionary biology, to give rise to a new epoch of biological researches.

  2. Савинов А.Б. Новая популяционная парадигма: популяция как симбиотическая самоуправляемая система // Вестн. Нижегород. ун-та им. Н.И. Лобачевского. Сер. Биология. 2005. Вып. 1 (9). С. 181–196. (http://macroevolution.narod.ru/savinov.htm)
    Савинов А.Б. Биосистемология (системные основы теории эволюции и экологии). Н.Новгород: Изд-во ННГУ, 2006. 205 с.
    (http://rogov.zwz.ru/Мacroevolution/savinov.doc)

  3. Dear Colleagues,
    I am very interested in the topic you are discussing.
    I would like to inform you that I in 2005 (see article Savinov, 2005) introduced the concepts of “autocenosis and« democenosis ».
    Autocenosis – a symbiotic system, which includes the host and its symbionts (prokaryotes and eukaryotes).
    Democenosis – a system of autocenosis.
    Based on these concepts I am trying to develop a symbiotic paradigm.

    Literature

    Savinov AB The new paradigm of population: population as a symbiotic self-governing system, “Vestn. Nizhny Novgorod. Univ NI Lobachevsky. Ser.Biology. 2005. Vol. 1 (9). S. 181-196. (http://macroevolution.narod.ru/savinov.htm)
    More on the topic look at my website:
    http://www.sabcor.dmls.ru/
    Yours sincerely,
    Dr. A. Savinov