It insects with sucking mouth parts such as

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Last updated: September 13, 2019

It is often easy to overlook the roles of microbes in terms of wider ecosystems, with such keenfocus on their human medicinal aspects. Not only do microbes have pivotal rolesin the maintenance of stability inecosystems on a large scale, but the applications of their intricate molecularfunctions can often induce outstanding biotechnological progress. With aparticular focus on the insect pathogenicfungi and plant symbiont Metarhizium acridum, this essay will aim to investigatethe role of the microbe in the ecosystem both as a pathogen and as anon-pathogenic symbiont, while applying its mechanisms and evolution to itspotential for advances in biotechnology.

 I will first explore how the dual life cycles of this fungi as a pathogenand an endophyte- a symbiont of a plant- are coupled by discussing theirmechanisms of action andevolutionary history. The mechanism of action is complex both in M. acridum’s role as an insect pathogen and endophyte. Asa pathogen, the mode of infection begins with penetration of the insectcuticle, by cuticular degradation using employment of enzymes such as proteasesand lipases(Pedrini et al.,2013; Barelli et al., 2015). This technique isnon-specific to M.

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acridum but opens the opportunity for the general family of insect-infecting fungi to infect a wider rangeof insects. The pathogens enter the insect’s body by the transgression of the cuticle rather thaningestion, meaning that insects with sucking mouthparts such as Aphids can also be affected (Chandler, 1997). The major proteases producedby the Metarhizium genus and used inthis way are Pr1A, a cuticle degrading subtilisin-like protease, and Pr2, a trypsin-like serine proteinase (St.

Leger, Joshi and Roberts, 1998). Not only do these proteasesplay a key role in penetration, but they also contribute to necessary evasionof host defences. This can be explained through research into how theyaided evasion of the host defence by degrading key antifungal proteins in theinsect (St Leger, Nelson and Screen, 1999).Following this, hydrophobicconidial spores adhere to the cuticle (Small and Bidochka, 2005). These then germinate, formingoutgrowing germ tubes and appressoria (Deising, Werner and Wernitz, 2000; Holder et al., 2007), which are then capable offurther penetration. It is the structure of these appressoria that link the roles of insect pathogenic fungi with thatof the plant symbiont. Deising et al.

(2000)identified that the appressoria present in the insect fungi showed significantsimilarity to those found in plant-infectingfungi. From this, we can speculate that there may be a morphological linkbetween the two, coupling their roles. The genus Metarhizium utilises the proteins MAD1 and ssgA tofacilitate adherence of the conidia onto the insect cuticle surfaces (St.

Leger, Staples and Roberts, 1992a; Wang and St.Leger, 2007a).A similar protein, MAD2 has beenfound to be responsible for adherence to plant surfaces (Wang and St. Leger, 2007). Once again, the presence ofeach of these genes suggests a dual role of the organism in the differenthosts.

OnceMetarhizium has finally entered themain body cavity- the haemocoel, expression of a collagen-like protein MCLI evades the immune system of theinsect (Wang and St Leger, 2006), allowing it to produce toxins and absorb nutrients,depleting them to fatal levels and eventually resulting in retreat of thefungal hyphae and mummification of the host (Small and Bidochka, 2005; Schrank and Vainstein,2010). Once inside the haemocoel, inorder to survive the osmotic pressure of the haemolymph in the host Metarhizium must adapt and it does thisthrough the expression of theosmosensor-like protein Mos1 (Wang, Duan and St. Leger, 2008).The mechanism of colonisation of M. acridum in plants as an endophyte isnot dissimilar to that of insect infection. Once again, the successfulassociation depends on adherence of the fungi to the plant surface, this timefacilitated by the protein MAD2 (Nicholson and Epstein, 1991; Wang and St.

Leger,2007).Sequencing of the Pr1 subtilisin-likeprotease indicated that this gene in the Metarhiziumwas, in fact, homologous to the protease At1 from grass endophyte Acremoniumtyphinum (Reddy, Lam and Belanger, 1996). This alternative fungalprotease At1 functions as afacilitator of plant colonisation by cell wall degradation. The similarity ofthese two proteases indicates a similar functional role of Metarhizium, enabling it tosuccessfully colonise as an endophyte. So why do the plant hosts’defence pathways not result in expulsion or death of these invasions? It has been found that fungal endophytes such as M. acridum are capable of communicatingwith the plant, indicating that they are in fact not pathogens. The moleculeresponsible for this, mycorrhizal factor(Myc) induces transcriptional andmorphological changes in the plant roots, such as activation of the symbioticsignalling pathway and increased root hair growth to raise the likelihood of contact between the fungal hyphaeand the plant roots (Maillet et al.

,2011).By doing this prior to and during rootcolonisation, the fungi are able to trickthe desired host into withdrawing its defencesand is then able to successfully carry outsymbiosis. Having looked in depth at themechanisms of the coupled functions of M.acridum, it is obvious that the fungus provides a multitude of beneficialservices to its ecosystem. The primary benefits to the plant hosts are simply that they acquire insect-derived nitrogen in areas where soilnitrogen may be limited (Behie, Zelisko and Bidochka, 2012)- they are therefore able toregain nitrogen lost to insects through herbivory. In return from the plant, M.

acridum is receiving access to simpleplant carbohydrates, those which are usually very difficult to access in thesoil due to being bound into complex carbohydrates such as cellulose andlignin. This discovery was outlined in workby Barelli et al. (2015), where theyintroduced 13CO2 to plants colonised with Metarhizium, tracking the 13C.Through doing this, they found that Metarhiziummutants lacking raffinose transporter gene mrt showed a reducedcompetency in the rhizosphere. This notonly leads us to the suggestion that carbon acquisition by fungi from planthosts is critical to their symbiotic relationship, but also that the mrt isa possible uptake route of these plant-derivedcarbohydrates. The acquisition of nitrogen, however, is not the only benefit ofM. acridum symbiosis for the plant.Increased foliage biomass in corn seeds, greater plant height and root length,and higher dry weights of shoots and roots are a few other proven benefits (Elena et al.

,2011; Liao et al., 2014). These would obviouslycontribute strongly to crop yield in agriculture, but also in terms of the natural ecosystem, herbivoreswould benefit from increased availability of food sources, leaving a cascadingabundance increase on their higher trophic levels.Alongside the beneficialecosystem services to the plant symbionts, we cannot ignore the negativeimpacts that exclusion of vital nutrients from the insects will ensue. As previously mentioned, eventual death and mummificationof the insects is the primary consequence of their pathogenesis, and on thelarge scale this could impact food webs by removal of M. acridum specific hosts such as locusts, and the broader hostranges of other species in the genus such as M. robertsii (Barelli et al.,2015).

  Reduction in herbivorypredation by depleted insect populations at the same time as the proliferation of plant abundance and yield withM. acridum and other similarsymbioses may mean that imbalance to food webs could lead to increases inabundance of primary consumers, and therefore declines in their other preywhich are not impacted by M. acridum. The key biotechnologicalapplications of M. acridum lie in thefields of agriculture and pharmaceuticals. Thepotential for individuals from the genera Metarhiziumand Beauveria to be used in thecontrol of insect pests in agricultural ecosystems has been known for over 100years, leading to the approval of many different formulations of these speciesto be used in protection of crops (Madelin etal.

, 1963; Faria and Wraight, 2007). Leading to the increased use and approval ofthese methods in pest control is a 2007 study by Kabaluk and Ericsson, in whichthey compared yields of corn from samples treated with only conventionalinsecticide with those treated with Metarhiziumin addition to the conventional technique. Theirfindings showed that the highest yield came undoubtedly from those which had beentreated with both treatments, not only showing progress from the previouslyused methods but also providing significant evidence to that aforementionedthat the Metarhizium symbiosis andits supply of nitrogen is the key factor implementing this increased health ofthe crop, rather than the removal of the insect pests, which was effectivelycarried out by the insecticide originally. A conversion from thesetraditional insecticidal treatments to those involving a larger amount ofnatural control through Metarhizium wouldhave positive climatic implications, reducing run-off of toxic chemicals fromthe insecticides which have potential to accumulate in organisms and also causedamaging eutrophication in aquatic systems.Pharmaceutical advances are another area wherebiotechnology of our example pathogen iscrucial.

Genomic data of Metarhiziumspecies compared to other fungi show enrichment of secondary metabolite geneclusters, with 52 core genes involved in the biosynthesisof secondary metabolites in M.acridium.Clusters of these important genes have been shown to have the potential for exploitation in biotransformationand biocatalysis, as well as in novel drug discovery. A study from 2014outlined the capability of endophytes such as M. acridum synthesising important metabolites with pharmaceuticalactivity when associated with their plant hosts.

An example of this they gave isTaxol, an anti-cancer drug that has been found to be present in the associationof endophytic fungi with yew trees(Garyali, Kumarand Reddy, 2014). The implication of this is that further areasof research are outlined, and with suchhigh diversity of microbes, not only endophytic fungi, present in the soilmicrobiome there seem limitlessexploitations in the case of secondary metabolites in novel drug synthesis. 

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