Pawnobes’: Cultivated commensal microbes that impact host phenotype

Thousands of years ago, humans went beyond hunting and gathering and began purposefully selecting and growing the most beneficial plants; what we know as the agricultural revolution was born. Is it possible that cultivating the microbiome would create a comparable paradigm shift?

The idea of consuming probiotics has received a lot of attention. Probiotics are not necessarily selected over numerous generations like domesticated crops; rather, they are often wild bacteria that are associated with favorable health. If wild bacteria happen to have a beneficial effect, this is little different than a wild plant that happens to be edible. Such an approach relies heavily on serendipitous observations and does not purposefully engineer probiotics that will improve complex multi-organism interactions.

In a new opinion paper [1], myself and collaborators discuss methods for beginning the process of microbe cultivation. For instance, stool transfers have already demonstrated so-called “super donors” who temporarily transmit marked improvement in insulin sensitivity to others [2]. To take this further, stool from a super donor could be transferred to many genetically similar, germ-free mice that would be observed for insulin sensitivity. Stool from the mice with the best traits could be transferred again to another set of germ-free mice and the process could continue until a more optimal stool transplant was developed.

This process will require careful methodological considerations that will be challenging at first. The same was true for the innovators who first started planting crops. Trial and error likely led to many failures before the first farmers developed methods for optimal cultivation. For instance, managing floods, droughts, pests, and weeds with the best tilling, planting, and fertilizing techniques must have involved challenging trade-offs. Over time, however, the methods, substrate, and products improved and generated a highly useful plant. In fact, the plant becomes so different from wild versions that biologists no longer use the same name to describe it. In both Kingdom Animalia and Kingdom Plantae, the products of artificial selection are called by different names (i.e. livestock and cultigen) from their wild ancestors.

We propose the microbial products of artificial selection should be named “pawnobes.” Based on the use of the word “pawn” in the game of chess and in other contexts, the term connotes small size, group function, and strategic manipulation. Group function is important because the interactions between pawnobes can also be selected for when all the organisms within a stool are transferred (i.e. beneficial synergies are intact at each transfer). Meanwhile, the suffix “–obe” identifies living organisms just as a microbe is a small living organism. Life changes over generations, allowing opportunities to select and transfer favorable changes.

Ultimately, the implications of these methods will likely go beyond human health to other scientific and engineering disciplines, as microbial synergies are also important in evolutionary biology, agriculture and elsewhere. Finally, artificial selection of pawnobes will need to proceed cautiously because (as demonstrated by artificial selection with antibiotics and pesticides) it may have unintended consequences.

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Acknowledgements:

The views expressed are those of the author and do not necessarily reflect the official policy or position of the Air Force, the Department of Defense, or the U.S. Government. Distribution A: Approved for public release; distribution is unlimited. Case Number: 88ABW-2015-3595, 16 Jul 2015.

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