Are we a mammal-microbial collective? Should we think of our interaction with our resident microbes as a harmonious, mutually helpful partnership, or a relationship gone sour?  In this podcast, I will lay out my case for why I think the (mutualistic) holobiont concept is often wrong headed and misleading.

Here is EvolutionMedicine ‘cast #6 for August 15th, ‘The Holobiont’:

Before proceeding further, let me first express my admiration for the point of view laid out in the recent paper “Getting the hologenome concept right, an eco-evolutionary framework for hosts and their microbiomes” (Theis et al. 2016).” My views align pretty well with the latter part of this paragraph:

“In The Hologenome Concept, some of us stated that “evolution of animals and plants was driven primarily by natural selection for cooperation between and with microorganisms” (Rosenberg and Zilber-Rosenberg  2013) while in other venues the concept “places as much emphasis on cooperation as on competition” (Rosenberg and Zilber-Rosenberg  2009) This latter statement is more precisely aligned with the pluralistic nature of the holobiont, namely that “natural selection…on holobiont phenotypes…can work to remove deleterious nuclear mutations or microbes while spreading advantageous nuclear mutations or microbes” (Bordenstein and Theis 2015). In fact, some of us argued that conflicts of interests resulting from the nature of the transmission of microbes to the next host could select for microbes that can manipulate the biology of their host to improve their own transmission (Dheilly et al. 2015)”

By contrast, Michael Shapira in a recent paper published in Trends in Ecology and Evolution argues that cooperation is the key to co-evolution of the host-microbiota collective. He writes: “overall, host–microbiota interactions describe a mutualistic symbiosis.”

I disagree.

It is this version of the holobiont point of view that I take issue with: natural selection for cooperation as a primary driver of the evolution of animals and plants. Instead my coauthors and I have argued that conflict is a more important driver.

Evidence for cooperation is exciting, fascinating, and necessary for the complete story of human-microbial association. But, these mutualistic interactions are not the most interesting or important, because they often fail to explain why diseases occur.

Mutualism is but one outcome of evolution acting on host and microbiome. Competition and conflict are equally likely, as we have argued here and here.

In diseases states,  our partnership with microbes is like a bad relationship:

Microbes consume you. They eat your lunch. And they invade your personal space.

Glossary:

Microbiome: collection of microbial genes in a host or other defined environment.

Microbiota: the collection of microorganisms resident in a host (or other environment).

Holobionts: the combined organism, made up of host & microbiota.

Hologenome: the combined host and microbial genes of a holobiont that may constitute a distinct and useful unit of selection that drives co-evolution.

References:

Copyright © Joe Alcock MD

Categories: Microbiome podcasts

Joe Alcock

Emergency Physician, Educator, Researcher, interested in the microbiome, evolution, and medicine