Pawnobiome: manipulation of the hologenome within one host generation and beyond

Abstract

A metaorganism is a collection of interacting organisms where the sum is not the same as the simple addition of the individual isolated parts (Relman, 2008; Webster, 2014). In fact, the gut, nasal, and lung microbiome all influence human phenotype (Redinbo, 2014). More specifically, the human gut microbiome has been linked to brain activity and to behavior (Collins et al., 2012). Similarly, Bacillus amyloliquefaciens supplementation improves feed conversion in chickens comparable to antibiotic growth promoters, by increasing villus height and crypt depth throughout the small intestine (Lei et al., 2015). It is apparent that phenotypic changes in the metaorganism influence the entire commensal unit.

The hologenome theory of evolution (HTE) asserts that a unit of selection is the holobiont which includes both the host and all its associated microbiota combined (Zilber-Rosenberg and Rosenberg, 2008). Some established components of the microbiota form a stable connection with the host; so, the entire holobiont is selected simultaneously with each passing host generation. The evolutionary fate of the holobiont unit is further linked with reliable vertical transmission of the microbiota whenever the host produces offspring.

The HTE is an important step forward in considering the evolutionary relevance of the wild-type microbiota, but it is not meant to characterize opportunities in deliberately manipulating and selecting microbes. Additionally, some microbes do not fit well within the HTE because they do not reliably transmit vertically, or they only influence host phenotype transiently. For instance, in one study, a yogurt probiotic altered bacterial carbohydrate metabolism markers without altering the species composition of the fecal bacteria (McNulty et al., 2011; Sanders et al., 2013). Similarly, fecal transplant appears promising for diabetes treatment, but thus far, has only been shown to improve insulin sensitivity temporarily (Vrieze et al., 2013). While a majority of the gut microbes in humans are stable day to day (Lozupone et al., 2012), only 60% of strains are durable beyond 5 years (Faith et al., 2013). These observations are the basis for our concept of the “Pawnobiome,” defined as the subset of the microbiome that is purposefully managed for manipulation of the host phenotype, which includes individual microbes named “pawnobes.”