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Anopheline mosquitoes are protected against parasite infection by tryptophan catabolism in gut microbiota

Nature Microbiology volume 7, pages 707–715 (2022)Cite this article

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Abstract

The mosquito microbiota can influence host physiology and vector competence, but a detailed understanding of these processes is lacking. Here we found that the gut microbiota of Anopheles stephensi, a competent malaria vector, is involved in tryptophan metabolism and is responsible for the catabolism of the peritrophic matrix impairing tryptophan metabolites. Antibiotic elimination of the microbiota led to the accumulation of tryptophan and its metabolites—kynurenine, 3-hydroxykynurenine (3-HK) and xanthurenic acid. Of these metabolites, 3-HK impaired the structure of the peritrophic matrix and promoted Plasmodium berghei infection. Among the major gut microbiota members in A. stephensi, Pseudomonas alcaligenes catabolized 3-HK as revealed by whole-genome sequencing and LC–MS metabolic analysis. The genome of P. alcaligenes encodes kynureninase (KynU) that is responsible for the conversion of 3-HK to 3-hydroxyanthranilic acid. Mutation of KynU resulted in a P. alcaligenes strain that was unable to metabolize 3-HK and unable to protect the peritrophic matrix. Colonization of A. stephensi with KynU-mutated P. alcaligenes failed to protect mosquitoes against parasite infection as compared with mosquitoes colonized with wild-type P. alcaligenes. In summary, this study identifies an unexpected function of mosquito gut microbiota in controlling mosquito tryptophan metabolism, with important implications for vector competence.

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Fig. 1: Microbiota-regulated Trp metabolism modulates P. berghei infection.
Fig. 2: 3-HK promotes Plasmodium infection via impairing the PM.
Fig. 3: Commensal P. alcaligenes catabolizes mosquito 3-HK.
Fig. 4: P. alcaligenes KynU degrades 3-HK in mosquitoes.

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Data availability

All data are available in the Article and its Supplementary information. The genomic sequence data of P. alcaligenes are available at the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) (accession no. PRJNA686701). Transcriptomic data are available at the NCBI SRA (accession no. PRJNA686698). The 16S rRNA gene sequences are available at the NCBI SRA (accession no. PRJNA686689). Source data are provided with this paper. Further information and requests for resources should be directed to J.W. (jingwenwang@fudan.edu.cn).

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Acknowledgements

We thank G. Zhang, C. Wang and J. Gou from Fudan University for technical advice on metabolites analysis; X. Zhou from Fudan University for support on statistical analysis; S. Zhao and H. Wang from Fudan University, and G. Dimopoulos from Johns Hopkins University for comments on the manuscript; and J. Yuan from Xiamen University for providing anti-P28 polyclonal antibody. This work was supported by the National Natural Science Foundation of China (U1902211) and the National Institutes of Health Grant (R01AI129819) to J.W.

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Author notes

  1. These authors contributed equally: Yuebiao Feng, Yeqing Peng, Xiumei Song, Han Wen.

Authors and Affiliations

  1. State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai, P. R. China

    Yuebiao Feng, Yeqing Peng, Xiumei Song, Han Wen, Yanpeng An, Huiru Tang & Jingwen Wang

  2. Zhongshan Hospital, Human Phenome Institute, Metabonomics and Systems Biology Laboratory at Shanghai International Centre for Molecular Phenomics, Fudan University, Shanghai, China

    Yeqing Peng, Yanpeng An & Huiru Tang

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Contributions

Y.F., Y.P., X.S., H.W., J.W. and H.T. designed experiments, interpreted results and wrote the paper. Y.P. and Y.A. performed metabolites analysis. X.S. and H.W. conducted PM structure analysis experiments. Y.F., X.S. and W.H. conducted bacteria recolonization and Plasmodium infection experiments. Y.F. conducted and analysed results from all additional experiments. J.W. and H.T. supervised the study. All authors discussed the results and commented on the manuscript.

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Correspondence to Huiru Tang or Jingwen Wang.

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Nature Microbiology thanks Louis Lambrechts, Flaminia Catteruccia and and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1. Tryptophan metabolites analysis post normal blood meal.

Relative amount of Trp metabolites in normal (N, n = 10) and antibiotics-treated (Abx, n = 10) mosquitoes 24 h post normal blood meal. Data are presented as mean ± s.e.m. Significance was determined by two-sided Student’s t-test.

Extended Data Fig. 2. Influence of microbiota on P. berghei infection and mosquito PM formation.

a, Oocyst numbers of Normal (N) and antibiotics-treated (Abx) mosquitoes. Horizontal black bars indicate the median values. Data were pooled from two independent experiments. Significance was determined by two-sided Mann-Whitney test. b, PAS staining of PM structure in N and Abx mosquitoes 45 h post normal blood meal at 100× and 200× magnification. Red arrows indicate the PM structure. Images are representative of at least six individual mosquito midguts. Scale bars represent 100 μm.

Extended Data Fig. 3. Knocking down HKT increases 3-HK level.

a, Relative expression levels of HKT in non-injected and dsRNA injected mosquitoes. The expression level of HKT was normalized to S7. The relative expression levels of HKT in dsHKT and dsGFP mosquitoes were normalized to the gene’s expression in non-injection group, respectively. Data are presented as mean ± s.e.m (n = 8). Results from one of two independent experiments are shown. b, Relative amount of 3-HK in dsGFP and dsHKT mosquitoes right before blood meal. Data are presented as mean ± s.e.m (n = 10). Significance was determined using ANOVA with Tukey’s test in (a) and two-sided Student’s t-test in (b).

Extended Data Fig. 4. Influence of 3-HK administration on An. stephensi survival and P. berghei exflagellation.

a, Fold change of 3-HK levels in control (n = 10) and 3-HK fed (n = 10) mosquitoes at 24 h (-24 h), 0 h (0 h) prior to and 24 h (24 h) post blood meal. Data are presented as mean ± s.e.m. b, Survival curve of control (n=46) and 3-HK fed (n=43) mosquitoes post an infectious blood meal. Results from one of two independent experiments are shown. c, Exflagellation rate monitored 15 min post infection in the control (-) and 3-HK fed (+) mosquitoes. Data were pooled from two independent experiments. Each dot represents an individual mosquito. Horizontal black bars indicate the median values (c). Significance was determined by two-sided Student’s t-test in (a), Log-rank (Mantel-Cox) test in (b) and Mann-Whitney test in (c).

Extended Data Fig. 5. Influence of 3-HK administration on midgut barrier function.

a, DHE staining of midguts in control (-) and 3-HK-treated (+) mosquitoes at 0 h prior to (left) and 24 h (right) post normal blood meal. Scale bars represent 100 μm. Images are representative of at least eight midguts. b, TUNEL staining of midgut from controls (-) and 3-HK-treated mosquitoes (+) at 0 h prior to (left) and 24 h (right) post normal blood meal. Scale bars represent 50 μm. Images are representative of at least four midguts. c, PH3 staining of midguts from controls (-) and 3-HK-treated (+) mosquitoes at 0 h (left) prior to and 24 h (right) post infectious blood meal. Scale bars represent 100 μm. d, Quantification of PH3-positive cells in the midguts at 0 h prior to infectious blood meal. Data are presented as mean ± s.e.m (n = 9). (e) Quantification of PH3-positive cells in the midguts from controls (n=4) and 3-HK-treated (n=5) mosquitoes at 24 h post infectious blood meal. Data are presented as mean ± s.e.m. Significance was determined by two-sided Student’s t-test.

Extended Data Fig. 6. Influence of 3-HK on Per1 expression.

a, Quantification of expression levels of Per1 in An. stephensi orally administrated 3-HK prior to blood feeding. Expression levels of Per1 were analyzed at 24 h (-24 h) and 0 h (0 h) prior to a blood meal in 3-HK treated and normal mosquitoes. Data are presented as mean ± s.e.m (n = 10). Results from one of two independent experiments are shown. b, Quantification of expression levels of Per1 in An. stephensi fed with blood and 3-HK simultaneously. Expression levels of Per1 were analyzed 24 h post a blood meal. Data are presented as mean ± s.e.m (n = 10). Results from one of two independent experiments are shown. Significance was determined by two-sided Student’s t-test.

Extended Data Fig. 7. Polyoxin D treatment abolishes the PM formation.

PAS staining of PM in normal mosquitoes (Control) (a, b), polyoxin D (PD) treated (c, d) and 3-HK + polyoxin D treated mosquitoes (3-HK+PD) (e, f) 45 h post normal blood meal at 100× and 200× magnification. Red arrows indicate the PM. Images are representative of at least three individual mosquito midguts. Scale bars represent 100 μm.

Extended Data Fig. 8. Trp supplementation impairs PM structure.

a, Western blot of Per1 in the midgut of Trp-treated (+) mosquitoes and control (-) 24 h post normal blood meal. b, Effect of Trp on P. berghei infection in Abx mosquitoes. Data were pooled from two independent experiments. Each dot represents an individual mosquito. Horizontal black bars indicate the median values. Significance was determined with a two-sided Mann-Whitney test.

Extended Data Fig. 9. Influence of P. alcaligenes on PM formation.

a, Phylogenetic tree showing the relationship between P. alcaligenes and other Pseudomonas sp. based on 16S rRNA gene sequences using ClustalW and MEGA. b, Fold change of P. alcaligenes abundance in the midguts of An. stephensi 0 h prior to and 24 h post normal blood meal. The level of 16S rRNA gene was normalized to that of s7 gene. Data are presented as mean ± s.e.m (n = 10). Significance was determined by two-sided Student’s t-test. Images are representative of two independent experiments. c, Colonization efficacy of P. alcaligenes in antibiotics- treated mosquitoes. P. alcaligenes CFU were counted in the midguts of Abx (-) and P. alcaligenes (+) recolonized mosquitoes before blood feeding. Data are presented as mean ± s.e.m (n = 5). d, PAS staining of PM in Abx and P. alcaligenes recolonized mosquitoes 45 h post normal blood meal at 100× and 200× magnification. Red arrows indicate the PM. Images are representative of at least seven individual mosquito midguts. Scale bars represent 100 μm.

Extended Data Fig. 10. Mutation of KynU in P. alcaligenes.

a, Confirmation of KynU deletion by PCR. b, The growth rate of wild type P. alcaligenes (P.a.WT) and KynU mutated P. alcaligenes (P.a.ΔKynU) in vitro. Data are presented as mean ± s.e.m (n = 6).

Supplementary information

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Supplementary Tables 1–3, 5 and 6, and Figs. 1 and 2.

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Supplementary Table 4

Differentially expressed genes between normal and 3-HK-treated mosquitoes.

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Feng, Y., Peng, Y., Song, X. et al. Anopheline mosquitoes are protected against parasite infection by tryptophan catabolism in gut microbiota. Nat Microbiol 7, 707–715 (2022). https://doi.org/10.1038/s41564-022-01099-8

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