1. Metarhizium fight club: Within-host competitive exclusion and resource partitioning.
- Author
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Sheng, Huiyu and St. Leger, Raymond J.
- Subjects
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PLANT exudates , *METARHIZIUM anisopliae , *INSECT pathogens , *AGRICULTURE , *PLANT colonization - Abstract
Both Metarhizium robertsii ARSEF 2575 (Mr2575) and Metarhizium anisopliae ARSEF 549 (Ma549) infect a range of insects whilst also interacting with plants; however, little is known about the traits that affect the competitive ability of different strains. We examined the interactions between Mr2575 and Ma549 in culture and during co-infection of plants (Arabidopsis thaliana) and insects. Mr2575 outcompetes Ma549 under nutrient-limiting conditions, including root exudates, giving it a priority advantage on Arabidopsis roots. However, during co-infection of Manduca sexta or Drosophila melanogaster, Ma549's higher blastospore production enhanced its competitive ability within the host. In large M. sexta (fifth instar), blastospores facilitate dispersal, suppress host melanization and prevent Mr2575 from spreading from infection sites, reducing conidia production. However, colonization of smaller hosts such as first instar M. sexta and D. melanogaster did not provide Ma549 with a competitive advantage, as conidial production was dependent on retaining control of the cuticle through which conidiating hyphae emerge. Unexpectedly, Ma549 and Mr2575 segregate within hosts, suggesting resource partitioning with Mr2575 predominating in the thoraxes of Drosophila, especially in females, and Ma549 in the abdomen. In fifth instar M. sexta, Mr2575 was most prevalent around spiracles and the front end of segments, despite Ma549 and Mr2575 having similar susceptibility to hypoxia. Dispersing conidia homogeneously into the hemocoel of fifth instar M. sexta eliminated the blastospore production advantage, making Ma549 and Mr2575 equally competitive, with strict partitioning of Mr2575 at the anterior and Ma549 at the posterior ends of segments. As Metarhizium species have multiple roles in natural ecosystems and agroecosystems these discoveries are relevant to understanding their impact on maintaining biodiversity and for exploiting them to enhance food security. Author summary: Metarhizium spp. are keystone fungi providing essential ecosystem services as plant symbionts and insect pathogens, yet little is known about how different strains interact. We analyzed two strains with different insect-killing strategies: Mr2575 kills insects with toxins before colonizing cadavers, whereas Ma549 rapidly colonizes living insects. Ma549's rapid growth within insects serves as a strong anti-competitive strategy in larger insects. However, in smaller insects, Mr2575 remains competitive in reproductive potential (spore production on cadavers) if it maintains control of the cuticle through which it entered the insect. Consequently, small hosts may be more critical than large hosts for preserving pathogen diversity. Unexpectedly, Mr2575 and Ma549 partition insect hosts between them, promoting coexistence. We also investigated trade-offs between virulence traits and plant colonization traits, finding that Mr2575's rapid growth in sparse nutrients enhances its competitiveness on plant roots. Thus, Mr2575 may be more competitive on plants, while Ma549 excels in large insects, with both strains showing similar competitiveness in small insects. These insights are important for understanding Metarhizium species' roles in biodiversity and their potential to boost food security in natural and agricultural ecosystems. [ABSTRACT FROM AUTHOR]
- Published
- 2024
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