Microbe Counts and Transgenerational Epigenetics

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Friday the 13th

 

90 per cent of you is not you. True?

My favorite statistic, as I have said here more than once, is this one: 9 out of 10 of your body cells are not “you” at all. They are microbes. Bacteria mostly, but the occasional odd member of other Kingdoms–notably fungi and archaea–as well. (We’re not counting viruses here, which would drive up those “not you” numbers enormously.)

That 9/10 figure is embedded in a lot of papers and textbooks, but even when there is a reference, the source is secondary. I concede that I have used it profligately without trying to nail it down precisely, hoping that all those papers and textbooks are enough to back me up.  It’s a statistic that belongs in the journalistic category of Too Good to Check.

Bioinformatician Neil Saunders is considerably more conscientious than I. He bravely went after the origin of the 9/10 data at his blog What You’re Doing is Rather Desperate.  (For an amusing–and profound–explanation of the blog title, see here.)

Saunders tracks the 9/10 statistic down to a 1971 article in the American Journal of Clinical Nutrition by one T.D. Luckey. A cool name. Saunders quoted from the paper: “Adult man carries 1012 microbes associated with his epidermis and 1014 microbes in his alimentary tract. . . The latter number is based upon 1011 microbes/g contents of an alimentary tract with a capacity of approximately 1 liter. The 1013 cells in his body are a distinct numerical minority of the total being that we call man. If we abandon anthropomorphism for the microbic view, we must admire the efficiency of these microbes in using man as a vehicle to further their own cause.”

Exactly. I am reminded of E.O. Wilson’s remark in Sociobiology: “the organism is only DNA’s way of making more DNA.”  Something similar might be said of our commensals: We lumbering apes are only the microbes’ way of making more microbes.

However, the comments to the Saunders post make a case that the 9/10 figure may not be accurate. One comment notes that the real number might be much higher because 9/10 is an extrapolation from bacteria that can be cultivated in the lab. A great many cannot be.

Another commenter argues that the true count might be lower because population sampling was from the gut and the skin, where microbes are most numerous. “The bacterial diversity and sheer numbers there are not even close to being representative of the rest of the body. What about the brain, or even the bladder?” “Liz” asked.

So, in the full knowledge that an accurate count of our resident microbes might be either considerably fewer than 9/10 or considerably more, I intend to go right on using that standard ratio. If it’s good enough for countless scientists, it’s good enough for me. The idea that 9 out of 10 of the cells I’m dragging around and nourishing in fact belong to other organisms is too astonishing give up.

 

Jean-Baptiste de Monet Chevalier de Lamarck (1744-1829)in about 1802, oil portrait by Charles Thévenin via Wikimedia Commons

Jean-Baptiste de Monet Chevalier de Lamarck (1744-1829) in about 1802, oil portrait by Charles Thévenin via Wikimedia Commons

Here comes Jean-Baptiste Lamarck?

This is about the research showing that male mice trained to fear a particular harmless smell–the cherry-smelling scent of acetophenone–before they sire offspring can pass the memory of that specific fear on to their children and grandchildren.

The research, published early this month, appears to be an example of transgenerational epigenetics.  Epigenetics is not a concept with a consensus definition, which is to say that just what it includes is a matter of scientific dispute. For our purposes, it’s enough to say that epigenetics encompasses a heterogeneous set of biochemical mechanisms that change the behavior of genetic material without changing any DNA sequences. Epigenetics seeks to explain how the environment turns genes off and on in particular cells at particular times. It’s about how nurture shapes nature.

Transgenerational epigenetics is, literally, epigenetics at a whole other level.  The idea is that epigenetic alterations acquired in one generation can be passed on to future generations. Transgenerational epigenetics is a pretty well-established phenomenon in plants. There is evidence that transgenerational epigenetics happens in animals, but it’s often controversial, especially when it is about our own species.

I blogged about the blogging about this paper earlier this week at the Genetic Literacy Project. (This post is based partly on that one.) A barrier to taking transgenerational epigenetics seriously is thinking up a mechanism to explain how such a crazy thing could happen. In the post I explore a couple of possibilities.

The day after that post I got the good news that BioScience, the journal of the American Institute of Biological Sciences, which is now in the sheltering arms of Oxford University Press, has gone open access. Yay for open access! Yay in particular for open-access BioScience, because it means you can now get easily to my two-part series on epigenetics. Marvelous timing. Part 1, covering the basics of epigenetics, appeared in 2009, but the basics haven’t changed much since then.  Part 2, published in 2011, focused on the epigenetics of behavior. It included a section on transgenerational epigenetics and the difficulties of studying it. 

 

A revolution in evolution?

Yesterday I ran across a post by Gregg Henriques, a psychologist blogging at Psychology Today. He greeted the new fear-of-smell paper with a hed calling it “A Revolution in Evolution.” He rhapsodizes: “From a psychological perspective, this is a HUGE finding. For starters, the idea of inter-generational trauma becomes much more complicated with an almost infinite number of possible causal pathways. At a more abstract level, the possibilities become truly remarkable—things like generational psychological legacies and notions such as Carl Jung’s collective unconscious archetypes, which might have seemed farfetched in the past, become more scientifically plausible.”

Whoa. Jung? Yikes.

An editorial in New Scientist wonders whether the smell of fear research means new respectability for a dirty word. The dirty word is “Lamarck.” That would be Jean-Baptiste Lamarck, the biologist whose work was mocked and rejected even in his own 18th century times. Henriques trots Lamarck out too.

Poor Lamarck, usually mocked and rejected today even though some of his work was praised by such illustrious figures as Stephen Jay Gould and Charles Darwin himself. Lamarck is most often associated with the supposedly discredited notion of inheritance of acquired characteristics. That’s the idea that traits taken on during life can be passed on to descendants. The oft-cited example, trotted out by both Henriques and New Scientist: “if giraffes stretch their necks to reach high leaves, their offspring have longer necks.”  The New Scientist editorialist says the fear memory work “seems consistent with Lamarckian inheritance . . . It fits with natural selection—and may yet give Lamarck’s name a sheen of respectability.”

 

No. Not natural selection. Not Lamarck either

About this, New Scientist and Henriques are mistaken. The smell of fear research really doesn’t fit with natural selection, at least not yet. Lamarckian inheritance of acquired characteristics has been controversial because the characteristics are supposed to be permanent. They shape evolution. All giraffes have long necks, and so do their descendants, even when they are snacking on greenery of moderate height.

The new paper describes the fear memory persisting in the grandchildren of the research subjects. There’s no claim that this process is affecting evolution. In fact, as far as I can tell, the length of this study contradicts none of the previous work on transgenerational epigenetics. When biological responses in one generation have been passed on to descendants, the changes characteristically don’t persist beyond three or four generations. They peter out.

In short, they do not become an example of evolution. The idea that a fear can be passed on to grandchildren through some so-far-unidentified biological mechanism is startling. But it is not really Lamarckian.

Not so far, anyway. Perhaps eventually there will be papers telling us what happens in the grandchildren of the affected grandchildren in this study. It would be pretty intriguing to learn that sixth-generation mice are also afraid of acetophenone. That news would certainly suggest an innate fear might be on the way to becoming a fixed evolutionary event.  The history of research on mammalian transgenerational epigenetics to date argues against it, but we’ll see.

There will almost certainly be papers attempting to replicate this work. Will they confirm it? Or contradict it? Mice have a relatively short generation time, so we might find out quite quickly whether the smell-of-fear results hold up.

 

Happy New Year

Time for the season of total family immersion. Have swell holidays.  See you next year, on January 10.

 

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