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Siderophore Biosynthesis but Not Reductive Iron Assimilation Is Essential for the Dimorphic Fungus Nomuraea rileyi Conidiation, Dimorphism Transition, Resistance to Oxidative Stress, Pigmented Microsclerotium Formation, and Virulence.

ABSTRACT: Iron is an indispensable factor for the dimorphic insect pathogenic Nomuraea rileyi to form persistent microsclerotia which can replace conidia or blastospores for commercial mass production. There are two high affinity iron acquisition pathways in N. rileyi, siderophore-assisted iron mobilization and reductive iron assimilation systems. Transcription of the two iron uptake pathways related genes is induced under iron-limiting conditions. Stage-specific iron uptake-related genes expression during microsclerotia development shows siderophore-mediated iron acquisition genes are rigorously upregulated specifically during the formation and mature period while reductive iron assimilation related genes just display a higher expression at the late maturation period. Abrogation of reductive iron assimilation, by the deletion of the high affinity iron permease (NrFtrA), has no visible effect on microsclerotia biogenesis in N. rileyi. In sharp contrast, N. rileyi L-ornithine-N(5)-monooxygenase (NrSidA), required for synthesis of all siderophores, is absolutely necessary for the development of pigmented microsclerotia. In agreement with the lower intracellular iron contents of microsclerotia in ?NrSidA strains, not only the pigments, but both the number and the biomass are also noticeably reduced. Certain concentration of ROS is required for promoting microsclerotia biogenesis. Combined with expression pattern analysis of related genes and quantitative of intracellular iron or extracellular siderophore in WT and mutants, these data demonstrate the lack of adequate intracellular iron caused by the loss of the siderophore results in the deficiency of ROS detoxication. Furthermore, ?NrSidA strains show significantly increased sensitivity to hydrogen peroxide. Besides, NrSidA, but not NrFtrA, play a crucial role in vegetative growth under iron-limiting conditions, conidiation, and dimorphic switching. Remarkably, the slower growth of the ?NrSidA strains in vivo due to a reduced capacity for iron acquisition leads to the loss of virulence in Spodoptera litura while the ?NrFtrA mutants behaved as WT during infection. Together, these results prove siderophore-assisted iron mobilization is the major pathway of cellular iron uptake and essential for conidiation, dimorphism transition, oxidative stress resistance, pigmented microsclerotium formation and full virulence.

SUBMITTER: Li Y

PROVIDER: S-EPMC4909778 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Siderophore Biosynthesis but Not Reductive Iron Assimilation Is Essential for the Dimorphic Fungus Nomuraea rileyi Conidiation, Dimorphism Transition, Resistance to Oxidative Stress, Pigmented Microsclerotium Formation, and Virulence.

Li Yan Y Wang Zhongkang Z Liu Xuee X Song Zhangyong Z Li Ren R Shao Changwen C Yin Youping Y

Frontiers in microbiology 20160616

Iron is an indispensable factor for the dimorphic insect pathogenic Nomuraea rileyi to form persistent microsclerotia which can replace conidia or blastospores for commercial mass production. There are two high affinity iron acquisition pathways in N. rileyi, siderophore-assisted iron mobilization and reductive iron assimilation systems. Transcription of the two iron uptake pathways related genes is induced under iron-limiting conditions. Stage-specific iron uptake-related genes expression durin ...[more]

PMID: 27379061

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Project description:Dimorphic plant and human mycopathogens require a switch from the usual yeast growth to filamentous growth for host tissue penetration, and the switch is controlled by multiple signaling systems other than the central developmental pathway. Unlike these fungi, dimorphic insect mycopathogens usually grow by hyphal extension, infect the host by hyphal penetration through the insect cuticle, and switch to unicellular blastospores from the penetrating hyphae only after entry into the host hemocoel, where blastospore propagation by yeast-like budding accelerates host mummification. Here, we report a dependence of the virulence-required dimorphic transition on the central pathway activators BrlA and AbaA in Beauveria bassiana Deletion of brlA or abaA abolished both aerial conidiation and submerged blastospore formation in vitro despite no negative impact on hyphal growth in various media, including a broth mimic of insect hemolymph. The hyphae of either deletion mutant lost insect pathogenicity through normal cuticle penetration, contrasting with a high infectivity of wild-type hyphae. The mutant hyphae injected into the host hemocoel failed to form blastospores, resulting in slower lethal action. Uncovered by transcriptomic analysis, several genes involved in host adhesion and cuticle degradation were sharply repressed in both deletion mutants versus wild type. However, almost all signaling genes homologous to those acting in the dimorphic switch of other fungi were not differentially expressed at a significant level and hence unlikely to be involved in shutting down the dimorphic switch of each deletion mutant. Therefore, like aerial conidiation, the submerged dimorphic switch in vitro and in vivo is a process of asexual development governed by the two central pathway activators in B. bassianaIMPORTANCE Dimorphic insect mycopathogens infect the host by hyphal penetration through the host cuticle and switch from the penetrating hyphae to unicellular blastospores after entry into the host hemocoel, where blastospore propagation by yeast-like budding accelerates host mummification to death. The fungal virulence-required dimorphic switch is confirmed as a process of asexual development directly regulated by BrlA and AbaA, two key activators of the central developmental pathway in an insect mycopathogen. This finding unveils a novel mechanism distinct from the control of the dimorphic switch by multiple signaling systems other than the central developmental pathway in dimorphic plant and human mycopathogens, which switch from the usual yeast growth to filamentous growth required for pathogenicity through host tissue penetration.

Dataset Information

Siderophore Biosynthesis but Not Reductive Iron Assimilation Is Essential for the Dimorphic Fungus Nomuraea rileyi Conidiation, Dimorphism Transition, Resistance to Oxidative Stress, Pigmented Microsclerotium Formation, and Virulence.

Publications

Siderophore Biosynthesis but Not Reductive Iron Assimilation Is Essential for the Dimorphic Fungus Nomuraea rileyi Conidiation, Dimorphism Transition, Resistance to Oxidative Stress, Pigmented Microsclerotium Formation, and Virulence.

Similar Datasets

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