Department of Entomology, University of Maryland, College Park, Maryland, United States of America.
PLoS Pathog. 2024 Nov 7;20(11):e1012639. doi: 10.1371/journal.ppat.1012639. eCollection 2024 Nov.
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.
罗伯茨绿僵菌 ARSEF 2575（Mr2575）和金龟子绿僵菌 ARSEF 549（Ma549）均可感染多种昆虫，同时也可与植物相互作用；然而，对于影响不同菌株竞争能力的特性，我们知之甚少。我们在培养过程中以及植物（拟南芥）和昆虫共感染时，研究了 Mr2575 和 Ma549 之间的相互作用。在营养有限的条件下，包括根分泌物，Mr2575 会胜过 Ma549，从而使其在拟南芥根部占据优先优势。然而，在烟粉虱或黑腹果蝇共感染时，Ma549 产生的大量孢子增强了其在宿主内的竞争能力。在大型烟粉虱（五龄幼虫）中，孢子有助于扩散，抑制宿主黑化，并阻止 Mr2575 从感染部位扩散，从而减少分生孢子的产生。然而，对于较小的宿主，如第一龄烟粉虱和黑腹果蝇，Ma549 并没有获得竞争优势，因为分生孢子的产生取决于对通过分生孢子产生的菌丝穿透的角质层的控制。出乎意料的是，Ma549 和 Mr2575 在宿主内分离，这表明通过 Mr2575 占主导地位的资源分配方式，特别是在雌性果蝇的胸部，而 Ma549 则在腹部。在五龄烟粉虱中，Mr2575 主要存在于果蝇的气门和节段前端，尽管 Ma549 和 Mr2575 对缺氧的敏感性相似。将分生孢子均匀地散布到五龄烟粉虱的血腔中，消除了孢子产生的优势，使 Ma549 和 Mr2575 具有同等的竞争力，Mr2575 严格分配在前部，Ma549 分配在节段的后部。由于金龟子属物种在自然生态系统和农业生态系统中具有多种作用，因此这些发现对于理解它们对维持生物多样性的影响以及利用它们来增强粮食安全具有重要意义。
