and weed out pieces of infected garden (Currie and Stuart 2001). As an additional
line of defence, leafcutter ants also interact extensively with antibiotic-producing
bacteria in the phylum Actinobacteria. These bacteria grow as a visible white mass
on specialised structures that are found on particular regions of the ants cuticle
(Currie et al. 1999b; Andersen et al. 2013; Kost et al. 2007; Currie et al. 2006).
Fueled by competition for the nutrients provided by the ant host, the bacterial
mutualists produce a variety of antibacterial and antifungal compounds. These
compounds have been shown to inhibit the growth of other microorganisms that
might invade the fungus garden, including the parasite E. weberi, and have also been
identified at active concentrations in the nests of leafcutter ants (Currie et al. 1999b,
2003; Barke et al. 2010; Haeder et al. 2009; Sen et al. 2009; Worsley et al. 2018;
Schoenian et al. 2011).
However, there is an interesting evolutionary twist to this story—E. weberi has
recently been shown to combat both of the ants two major lines of defence. The
parasite has evolved to produce chemicals, called shearinine D and melinacidin IV,
that not only prevent the weeding behaviours of the ants by causing paralysis and
eventual mortality, but that also inhibit the growth of the actinobacterial symbionts
(Heine et al. 2018). Despite this, widespread resistance does not seem to be the case
in nature and the attine-actinobacteria mutualism is thought to have survived and
enabled ants to farm their fungus for over 50 millions years (Currie et al. 2006).
Instead, a constant coevolutionary arms race seems to be occurring within the
leafcutter ant system, involving the Escovopsis parasite, the ants, and their protective
symbionts. The evolution of resistance in Escovopsis drives the evolution of novel
antimicrobial compounds in the mutualistic Actinobacteria and therefore prevents
the dominance of resistant parasite strains (Currie et al. 2006; Pathak et al. 2019;
Worsley et al. 2018). Additionally, different actinobacterial species on the ants’
cuticle produce different types of antimicrobial compound, resulting in a form of
multidrug therapy whereby parasites are faced with too many compounds to evolve
resistance to all of them at once (Barke et al. 2010; Seipke et al. 2011).
23.2.2 Actinobacteria as Protective Symbionts
Leafcutter ants are not alone in recruiting antibiotic-producing Actinobacteria to
protect against disease. In fact, Actinobacteria are thought to be involved in approximately half of all described examples of defensive mutualism (Kaltenpoth 2009)
and interact with a range of terrestrial and marine invertebrates, as well as several
plant host species (Kaltenpoth 2009; Seipke et al. 2012; Viaene et al. 2016). Apart
from having a diverse secondary metabolism capable of producing many antimicrobial natural products, Actinobacteria are also characterised by a lifecycle involving
filamentous growth and spore-forming stages. Members of this phylum are also
capable of subsisting on a wide range of carbon sources and metabolic waste
products that are often present at very low concentrations. Together, these characteristics may have enabled Actinobacteria to interact with a diverse range of hosts
500
S. Worsley
line of defence, leafcutter ants also interact extensively with antibiotic-producing
bacteria in the phylum Actinobacteria. These bacteria grow as a visible white mass
on specialised structures that are found on particular regions of the ants cuticle
(Currie et al. 1999b; Andersen et al. 2013; Kost et al. 2007; Currie et al. 2006).
Fueled by competition for the nutrients provided by the ant host, the bacterial
mutualists produce a variety of antibacterial and antifungal compounds. These
compounds have been shown to inhibit the growth of other microorganisms that
might invade the fungus garden, including the parasite E. weberi, and have also been
identified at active concentrations in the nests of leafcutter ants (Currie et al. 1999b,
2003; Barke et al. 2010; Haeder et al. 2009; Sen et al. 2009; Worsley et al. 2018;
Schoenian et al. 2011).
However, there is an interesting evolutionary twist to this story—E. weberi has
recently been shown to combat both of the ants two major lines of defence. The
parasite has evolved to produce chemicals, called shearinine D and melinacidin IV,
that not only prevent the weeding behaviours of the ants by causing paralysis and
eventual mortality, but that also inhibit the growth of the actinobacterial symbionts
(Heine et al. 2018). Despite this, widespread resistance does not seem to be the case
in nature and the attine-actinobacteria mutualism is thought to have survived and
enabled ants to farm their fungus for over 50 millions years (Currie et al. 2006).
Instead, a constant coevolutionary arms race seems to be occurring within the
leafcutter ant system, involving the Escovopsis parasite, the ants, and their protective
symbionts. The evolution of resistance in Escovopsis drives the evolution of novel
antimicrobial compounds in the mutualistic Actinobacteria and therefore prevents
the dominance of resistant parasite strains (Currie et al. 2006; Pathak et al. 2019;
Worsley et al. 2018). Additionally, different actinobacterial species on the ants’
cuticle produce different types of antimicrobial compound, resulting in a form of
multidrug therapy whereby parasites are faced with too many compounds to evolve
resistance to all of them at once (Barke et al. 2010; Seipke et al. 2011).
23.2.2 Actinobacteria as Protective Symbionts
Leafcutter ants are not alone in recruiting antibiotic-producing Actinobacteria to
protect against disease. In fact, Actinobacteria are thought to be involved in approximately half of all described examples of defensive mutualism (Kaltenpoth 2009)
and interact with a range of terrestrial and marine invertebrates, as well as several
plant host species (Kaltenpoth 2009; Seipke et al. 2012; Viaene et al. 2016). Apart
from having a diverse secondary metabolism capable of producing many antimicrobial natural products, Actinobacteria are also characterised by a lifecycle involving
filamentous growth and spore-forming stages. Members of this phylum are also
capable of subsisting on a wide range of carbon sources and metabolic waste
products that are often present at very low concentrations. Together, these characteristics may have enabled Actinobacteria to interact with a diverse range of hosts
500
S. Worsley