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Transferrin-mediated iron sequestration suggests a novel therapeutic strategy for controlling Nosema disease in the honey bee, Apis mellifera

Rodríguez-García, Cristina, Heerman, Matthew C., Cook, Steven C., Evans, Jay D., DeGrandi-Hoffman, Gloria, Banmeke, Olubukola, Zhang, Yi, Huang, Shaokang, Hamilton, Michele, Chen, Yan Ping·2021·PLOS Pathogens
DOI 10.1371/journal.ppat.1009270PMC PMC7891791
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Abstract

Nosemosis C, a Nosema disease caused by microsporidia parasite Nosema ceranae, is a significant disease burden of the European honey bee Apis mellifera which is one of the most economically important insect pollinators. Nevertheless, there is no effective treatment currently available for Nosema disease and the disease mechanisms underlying the pathological effects of N. ceranae infection in honey bees are poorly understood. Iron is an essential nutrient for growth and survival of hosts and pathogens alike. The iron tug-of-war between host and pathogen is a central battlefield at the host-pathogen interface which determines the outcome of an infection, however, has not been explored in honey bees. To fill the gap, we conducted a study to investigate the impact of N. ceranae infection on iron homeostasis in honey bees. The expression of transferrin, an iron binding and transporting protein that is one of the key players of iron homeostasis, in response to N. ceranae infection was analysed. Furthermore, the functional roles of transferrin in iron homeostasis and honey bee host immunity were characterized using an RNA interference (RNAi)-based method. The results showed that N. ceranae infection causes iron deficiency and upregulation of the A. mellifera transferrin (AmTsf) mRNA in honey bees, implying that higher expression of AmTsf allows N. ceranae to scavenge more iron from the host for its proliferation and survival. The suppressed expression levels of AmTsf via RNAi could lead to reduced N. ceranae transcription activity, alleviated iron loss, enhanced immunity, and improved survival of the infected bees. The intriguing multifunctionality of transferrin illustrated in this study is a significant contribution to the existing body of literature concerning iron homeostasis in insects. The uncovered functional role of transferrin on iron homeostasis, pathogen growth and honey bee’s ability to mount immune responses may hold the key for the development of novel strategies to treat or prevent diseases in honey bees.

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Figures

Fig 1 Graphic representation of the study design for field colonies.
Fig 1 Graphic representation of the study design for field colonies.CC0 · PubMed Central
Fig 2 Graphic representation of the study design for laboratory cage assay.
Fig 2 Graphic representation of the study design for laboratory cage assay.CC0 · PubMed Central
Fig 3 Expression levels of N. ceranae 16S rRNA. The transcriptional activity of N. ceranae 16S rRNA was corresponding with the level of spore loads in infected bees. The relative expression of N. ceranae 16S rRNA in forager bees was significantly higher than in nurse bees under both high- and low- levels of infection (1.2 M vs 26 M N. ceranae spores per bee). The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and an asterisk (*) denotes a statistically significant difference between the two groups (P ≤ 0.05, Student’s t-test).
Fig 3 Expression levels of N. ceranae 16S rRNA. The transcriptional activity of N. ceranae 16S rRNA was corresponding with the level of spore loads in infected bees. The relative expression of N. ceranae 16S rRNA in forager bees was significantly higher than in nurse bees under both high- and low- levels of infection (1.2 M vs 26 M N. ceranae spores per bee). The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and an asterisk (*) denotes a statistically significant difference between the two groups (P ≤ 0.05, Student’s t-test).CC0 · PubMed Central
Fig 4 Tissue specific total amount of iron in gut and fat body tissues of nurse and forager bees. An asterisk (*) denotes a statistically significant difference between the two groups (p ≤ 0.05).
Fig 4 Tissue specific total amount of iron in gut and fat body tissues of nurse and forager bees. An asterisk (*) denotes a statistically significant difference between the two groups (p ≤ 0.05).CC0 · PubMed Central
Fig 5 Tissue-specific relative transferrin mRNA transcript level in gut and fat body tissues of nurse forager bees. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and an asterisk (*) denotes a statistically significant difference between the two groups (P ≤ 0.05).
Fig 5 Tissue-specific relative transferrin mRNA transcript level in gut and fat body tissues of nurse forager bees. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and an asterisk (*) denotes a statistically significant difference between the two groups (P ≤ 0.05).CC0 · PubMed Central
Fig 6 The relative expression of transferrin after treatment of AmTsf -dsRNA. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).
Fig 6 The relative expression of transferrin after treatment of AmTsf -dsRNA. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).CC0 · PubMed Central
Fig 7 The relative expression of N. ceranae 16S rRNA after treatment of AmTsf -dsRNA. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).
Fig 7 The relative expression of N. ceranae 16S rRNA after treatment of AmTsf -dsRNA. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).CC0 · PubMed Central
Fig 8 Total amount of iron in bees on day 6 and day 12 post AmTsf -dsRNA treatment. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).
Fig 8 Total amount of iron in bees on day 6 and day 12 post AmTsf -dsRNA treatment. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).CC0 · PubMed Central
Fig 9 Time dependent transcription profiles for genes encoding antimicrobial immune peptides. (A) Apidaecin, (B) Abaecin, and (C) for gene encoding inhibitor of apoptosis Birc5. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).
Fig 9 Time dependent transcription profiles for genes encoding antimicrobial immune peptides. (A) Apidaecin, (B) Abaecin, and (C) for gene encoding inhibitor of apoptosis Birc5. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).CC0 · PubMed Central
Fig 10 Transcript levels for RNA-induced silencing complex components. (A) Argonaute. (B) Dicer. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).
Fig 10 Transcript levels for RNA-induced silencing complex components. (A) Argonaute. (B) Dicer. The relative expression was expressed as an n-fold difference relative to the calibrator (marked by a star) by 2–∆∆Ct method. A star denotes a calibrator and the different lower-case letters above bars indicate the statistically significant difference among different groups (P ≤ 0.05, ANOVA and Tukey´s tests).CC0 · PubMed Central
Fig 11 Kaplan–Meier survival curves for the three experimental groups (N = 90 bees/group). Data represent percentage of survival for the four groups over 12 days of experimental observation. Group I: Nosema-infected bees (infected/untreated); Group II: Nosema-infected bees + AmTsf -dsRNA treatment (infected/treated); Group III: Healthy bees (uninfected/untreated) and Group IV: Nosema-infected bees + GFP-dsRNA. Knockdown of the honey bee transferrin gene reduced the incidence of death (p< 0.05 by Wilcoxon test <p = 0.0041> and Log-rank test <P = 0.0033>).
Fig 11 Kaplan–Meier survival curves for the three experimental groups (N = 90 bees/group). Data represent percentage of survival for the four groups over 12 days of experimental observation. Group I: Nosema-infected bees (infected/untreated); Group II: Nosema-infected bees + AmTsf -dsRNA treatment (infected/treated); Group III: Healthy bees (uninfected/untreated) and Group IV: Nosema-infected bees + GFP-dsRNA. Knockdown of the honey bee transferrin gene reduced the incidence of death (p< 0.05 by Wilcoxon test <p = 0.0041> and Log-rank test <P = 0.0033>).CC0 · PubMed Central

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Cited by

Sorted by citations

Metadata

Authors
Rodríguez-García, C., Heerman, M. C., Cook, S. C., Evans, J. D., DeGrandi-Hoffman, G., Banmeke, O., Zhang, Y., Huang, S., Hamilton, M., & Chen, Y. P.
ORCID
Venue
PLOS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2021-02-18
Volume
17
Issue
2
Pages
e1009270
ISSN
1553-7374
DOI
10.1371/journal.ppat.1009270
PMC
PMC7891791
Cited by
50
References
7
Language
en
Licence
creativecommons.org/publicdomain/zero/1.0/ (vor)

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