23.3 Selecting Protective Microbes
In many cases, protective microorganisms appear to be a consistent part of, or even
dominate, the host microbiome. For example, Actinobacteria massively outnumber
other microbial species on the cuticles of leafcutter ants (Andersen et al. 2013) and
Bifidobacteria dominate the infant human gut, where they inhibit the growth of
pathogens and promote immune system development (Matamoros et al. 2013). A
great challenge is to understand how a host can selectively associate with these
microbial species when it is exposed to a huge environmental pool of microbes. Such
knowledge could enable us to enhance the presence of beneficial microbes, for
example in the human gut following a course of antibiotics, or in the roots of
economically important crop plant species to reduce yield losses caused by disease.
23.3.1 The ‘Partner Choice Problem’
The issue of how a host recruits specific microbes is often referred to as the ‘partner
choice problem’. This is because for a host to be able to accumulate beneficial
species, it must be able to distinguish between different strains in its environment
and limit its interactions to microbes that provide it with significant benefits (Archetti
et al. 2011). For many instances of partner choice in nature individuals can distinguish between better or worse partners via costly phenotypes. For example, elaborate
male ornaments, such as tail feathers, facilitate mate choice in many bird species,
since only high-quality individuals can afford to invest in these (Archetti et al. 2011).
However, with microbial-host interactions, it seems unlikely that such signals could
exist and be detected by the host, allowing discrimination between thousands of
microbial species. Instead other mechanisms are thought to enable hosts to indirectly
bias the accumulation of beneficial microbial species from their environment
(Archetti et al. 2011; Boza et al. 2019; Scheuring and Yu 2012).
One mechanism by which a host could encourage the colonisation of protective
species within its microbiome is by giving certain microbes preferential access to
resources in the host niche. The simplest way by which this can occur is by
transmitting them vertically across host generations, rather than acquiring them
horizontally from the environment (Boza et al. 2019). This is the case for leafcutter
ants, which remain sterile before they hatch from the pupal stage (Marsh et al. 2014).
Following hatching, they are inoculated with the antibiotic-producing
Actinobacteria that grow on older worker ants, within a 24 h window (Marsh et al.
2014). These filamentous Actinobacteria then bloom over the ant cuticle in the
absence of any competition, before receding to grow around specialised crypts
which are thought to supply the cuticular microbiome with resources (Currie et al.
2006).
A second mechanism by which a host could drive the accumulation of beneficial
microbial species is by providing its microbiome with specific nutrients that are
23 Defensive Microbiomes: A Widespread Phenomenon in Nature
503
In many cases, protective microorganisms appear to be a consistent part of, or even
dominate, the host microbiome. For example, Actinobacteria massively outnumber
other microbial species on the cuticles of leafcutter ants (Andersen et al. 2013) and
Bifidobacteria dominate the infant human gut, where they inhibit the growth of
pathogens and promote immune system development (Matamoros et al. 2013). A
great challenge is to understand how a host can selectively associate with these
microbial species when it is exposed to a huge environmental pool of microbes. Such
knowledge could enable us to enhance the presence of beneficial microbes, for
example in the human gut following a course of antibiotics, or in the roots of
economically important crop plant species to reduce yield losses caused by disease.
23.3.1 The ‘Partner Choice Problem’
The issue of how a host recruits specific microbes is often referred to as the ‘partner
choice problem’. This is because for a host to be able to accumulate beneficial
species, it must be able to distinguish between different strains in its environment
and limit its interactions to microbes that provide it with significant benefits (Archetti
et al. 2011). For many instances of partner choice in nature individuals can distinguish between better or worse partners via costly phenotypes. For example, elaborate
male ornaments, such as tail feathers, facilitate mate choice in many bird species,
since only high-quality individuals can afford to invest in these (Archetti et al. 2011).
However, with microbial-host interactions, it seems unlikely that such signals could
exist and be detected by the host, allowing discrimination between thousands of
microbial species. Instead other mechanisms are thought to enable hosts to indirectly
bias the accumulation of beneficial microbial species from their environment
(Archetti et al. 2011; Boza et al. 2019; Scheuring and Yu 2012).
One mechanism by which a host could encourage the colonisation of protective
species within its microbiome is by giving certain microbes preferential access to
resources in the host niche. The simplest way by which this can occur is by
transmitting them vertically across host generations, rather than acquiring them
horizontally from the environment (Boza et al. 2019). This is the case for leafcutter
ants, which remain sterile before they hatch from the pupal stage (Marsh et al. 2014).
Following hatching, they are inoculated with the antibiotic-producing
Actinobacteria that grow on older worker ants, within a 24 h window (Marsh et al.
2014). These filamentous Actinobacteria then bloom over the ant cuticle in the
absence of any competition, before receding to grow around specialised crypts
which are thought to supply the cuticular microbiome with resources (Currie et al.
2006).
A second mechanism by which a host could drive the accumulation of beneficial
microbial species is by providing its microbiome with specific nutrients that are
23 Defensive Microbiomes: A Widespread Phenomenon in Nature
503