of these microbial communities in great detail and many studies have demonstrated
that there are often consistent patterns in the microbial groups that associate with a
particular host species. For example, in humans the early-life infant gut is almost
always dominated by certain species of the bacterial genus Bifidobacterium, which
are then superseded by members of the phyla Firmicutes and Bacteriodetes later in
adult life (Matamoros et al. 2013). Furthermore, several microbial communities, for
example those associated with plants and insects, have been found to be tightly
linked to host phylogeny, suggesting that particular microbial assemblages are
maintained and are changing over evolutionary time alongside their host (Brucker
and Bordenstein 2012; Fitzpatrick et al. 2018; Sanders et al. 2014).
The non-random accumulation of microbial communities within the host
microbiome suggests that host species may be able to influence which microorganisms they associate with. In fact, hosts are expected to experience strong natural
selection to filter the enormous pool of microbial species available to them and
evolve mechanisms that encourage the persistence of microbes that provide them
with significant fitness benefits (Archetti et al. 2011; Foster et al. 2017; Scheuring
and Yu 2012). Microorganisms can be advantageous to their host in a number of
different ways. For example, many provide their hosts with nutritional benefits by
breaking down complex, otherwise indigestible molecules, or by supplementing the
host diet with essential nutrients through pathways such as nitrogen fixation or
phosphate solubilisation. Other symbionts, which are the focus of this essay, can
provide protective benefits to their host by inhibiting the growth and invasion of
pathogenic and parasitic organisms.
23.2.1 Leafcutter Ants and Their Protective Microbes
Attine leafcutter ants represent a fascinating example of a defensive mutualism
between antimicrobial-producing bacteria and a eukaryotic host. Leafcutter ants
are indigenous to Central and Southern America and are renowned for their
specialised agricultural activities. Worker ants collect fresh leaf material from their
surrounding environment which is then taken back to their nests and used as a
compost to grow a mutualistic food fungus, called Leucoagaricus gongylophorous
(Worsley et al. 2018; Currie 2001). In return for a growth substrate, the fungus
produces swellings called gongylidia which are rich in lipids and proteins. These are
harvested by the ants and used as the sole nutrients source for the queen and her
larvae (De Fine Licht et al. 2014; Currie 2001).
Although this system is effective, the clonal fungal cultivar is a rich food source
and is therefore at risk from being parasitised by other organisms. Indeed, another
fungus called Escovopsis weberi is highly specialised to grow on the food fungus
and, if left unchecked, can cause ant colony collapse. This occurs when the ants are
starved of their food source and eventually die or abandon their nest (Currie et al.
1999a; de Man et al. 2016). However, the ants have evolved several lines of defence
against such invasions, including specialised behaviours that enable them to detect
23 Defensive Microbiomes: A Widespread Phenomenon in Nature
499
that there are often consistent patterns in the microbial groups that associate with a
particular host species. For example, in humans the early-life infant gut is almost
always dominated by certain species of the bacterial genus Bifidobacterium, which
are then superseded by members of the phyla Firmicutes and Bacteriodetes later in
adult life (Matamoros et al. 2013). Furthermore, several microbial communities, for
example those associated with plants and insects, have been found to be tightly
linked to host phylogeny, suggesting that particular microbial assemblages are
maintained and are changing over evolutionary time alongside their host (Brucker
and Bordenstein 2012; Fitzpatrick et al. 2018; Sanders et al. 2014).
The non-random accumulation of microbial communities within the host
microbiome suggests that host species may be able to influence which microorganisms they associate with. In fact, hosts are expected to experience strong natural
selection to filter the enormous pool of microbial species available to them and
evolve mechanisms that encourage the persistence of microbes that provide them
with significant fitness benefits (Archetti et al. 2011; Foster et al. 2017; Scheuring
and Yu 2012). Microorganisms can be advantageous to their host in a number of
different ways. For example, many provide their hosts with nutritional benefits by
breaking down complex, otherwise indigestible molecules, or by supplementing the
host diet with essential nutrients through pathways such as nitrogen fixation or
phosphate solubilisation. Other symbionts, which are the focus of this essay, can
provide protective benefits to their host by inhibiting the growth and invasion of
pathogenic and parasitic organisms.
23.2.1 Leafcutter Ants and Their Protective Microbes
Attine leafcutter ants represent a fascinating example of a defensive mutualism
between antimicrobial-producing bacteria and a eukaryotic host. Leafcutter ants
are indigenous to Central and Southern America and are renowned for their
specialised agricultural activities. Worker ants collect fresh leaf material from their
surrounding environment which is then taken back to their nests and used as a
compost to grow a mutualistic food fungus, called Leucoagaricus gongylophorous
(Worsley et al. 2018; Currie 2001). In return for a growth substrate, the fungus
produces swellings called gongylidia which are rich in lipids and proteins. These are
harvested by the ants and used as the sole nutrients source for the queen and her
larvae (De Fine Licht et al. 2014; Currie 2001).
Although this system is effective, the clonal fungal cultivar is a rich food source
and is therefore at risk from being parasitised by other organisms. Indeed, another
fungus called Escovopsis weberi is highly specialised to grow on the food fungus
and, if left unchecked, can cause ant colony collapse. This occurs when the ants are
starved of their food source and eventually die or abandon their nest (Currie et al.
1999a; de Man et al. 2016). However, the ants have evolved several lines of defence
against such invasions, including specialised behaviours that enable them to detect
23 Defensive Microbiomes: A Widespread Phenomenon in Nature
499