Hindgut Innate Immunity and Regulation of Fecal Microbiota through Melanization in Insects

Shao, Qi-Miao; Yang, Bing; Xu, Qiufang; Li, Xuquan; Lu, Zhiqiang; Wang, Chengshu; Huang, Yang; Söderhäll, Kenneth; Ling, Erjun

doi:10.1074/jbc.m112.354548

Cited by 105 publications

(104 citation statements)

References 30 publications

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“…Melanin generated from the precursors of dopa and dopamine by the activated phenol oxidases (POs) is important for immune responses [5, 7–9, 12, 14–16, 19, 23, 24, 55, 56]. Genes ( TH , DDC etc . )…”

Section: Discussionmentioning

confidence: 99%

Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae)

Zeng

Hao

et al. 2017

Parasites Vectors

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BackgroundPhenol oxidases (POs) catalyze the oxidation of dopa and dopamine to melanin, which is crucial for cuticle formation and innate immune maintenance in insects. Although, Laccase 2, a member of the PO family, has been reported to be a requirement for melanin-mediated cuticle tanning in the development stages of some insects, whether it participates in cuticle construction and other physiological processes during the metamorphosis of mosquito pupae is unclear.MethodsThe association between the phenotype and the expression profile of Anopheles sinensis Laccase 2 (AsLac2) was assessed from pupation to adult eclosion. Individuals showing an expression deficiency of AsLac2 that was produced by RNAi and their phenotypic defects and physiological characterizations were compared in detail with the controls.ResultsDuring the dominant expression period, knockdown of AsLac2 in pupae caused the cuticle to be unpigmented, and produced thin and very soft cuticles, which further impeded the eclosion rate of adults as well as their fitness. Moreover, melanization immune responses in the pupae were sharply decreased, leading to poor resistance to microorganism infection. Both the high conservation among Laccase 2 homologs and a very similar genomic synteny of the neighborhood in Anopheles genus implies a conservative function in the pupal stage.ConclusionsTo our knowledge, this is the first study to report the serious phenotypic defects in mosquito pupae caused by the dysfunction of Laccase 2. Our findings strongly suggest that Laccase 2 is crucial for Anopheles cuticle construction and melanization immune responses to pathogen infections during pupal metamorphosis. This irreplaceability provides valuable information on the application of Lacccase 2 and/or other key genes in the melanin metabolism pathway for developing mosquito control strategies.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2118-4) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae)

Zeng

Hao

et al. 2017

Parasites Vectors

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“…Approximately 15 μg total proteins were loaded for denaturing SDS-PAGE separation followed by Coomassie Brilliant Blue R-250 staining. Based on the molecular sizes of cuticle proteins listed in Additional file 2: Table S2, the gels that appeared to contain cuticle proteins were excised for LC-MS/MS assay as previously described [4]. The two databases used in this study were SilkDB (http://silkworm.genomics.org.cn/) and the B. mori protein sequence database which was downloaded from NCBI (www.ncbi.nlm.nih.gov) using the keyword “ Bombyx mori ”.…”

Section: Methodsmentioning

confidence: 99%

“…Food debris is then transferred to the hindgut for water, salt, and some nutrient absorption [3]. In herbivorous insects such Bombyx mori , prophenoloxidase (PPO) produced by hindgut epidermal cells eliminates the majority of microorganisms in the food debris by inducing melanization of feces, thus avoiding the distribution of potential pathogens into the surrounding habitat [4]. In the insect foregut, there is also PPO that can detoxify food phenolics [5].…”

Section: Introductionmentioning

confidence: 99%

Analysis of gene expression in the midgut of Bombyx mori during the larval molting stage

et al. 2016

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BackgroundInsects can be models for understanding human intestinal infection and pathology. Molting, a special period during which the old insect cuticle is shed and a new one is produced, is crucial for insect development. Holometabolous insects may experience several larva-to-larva moltings to become larger, a pupal molt and adult eclosion to become adults. During the larval molts, they stop feeding and become quiescent. Although the molting larvae become quiescent, it is not known if changes in microbiome, physiology, development and immunity of midguts occur.ResultsTranscriptome analysis indicated that functions such as metabolism, digestion, and transport may become reduced due to the downregulated expression of many associated genes. During the molting stage, midguts harbor less microflora and DNA synthesis decreases. Both ecdysone and juvenile hormone in the larval midgut likely degrade after entering the larva-to-larva molting stage. However, at 12 h after ecdysis, the feeding larvae of 5th instars that were injected with 20-hydroxyecdysone entered a molting-like stage, during which changes in midgut morphology, DNA synthesis, gene expression, and microflora exhibited the same patterns as observed in the actual molting state.ConclusionThis study is important for understanding insect midgut physiology, development and immunity during a special development stage when no food is ingested. Although the molting larva becomes immobile and quiescent, we demonstrate that numerous changes occur in midgut morphology, physiology, metabolism and microbiome during this period.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3162-8) contains supplementary material, which is available to authorized users.

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“…Gut-associated bacteria can influence insect dietary preferences (4,19) and are reciprocally regulated by immune genes and enzymes of the hosts (20)(21)(22). Interestingly, microarray studies of RR-and WT-WCR adult heads have identified differentially expressed sequence tags showing sequence similarity with immune proteins (23).…”

mentioning

confidence: 99%

Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm

Chu

Spencer

Curzi

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

129

114

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Insects are constantly adapting to human-driven landscape changes; however, the roles of their gut microbiota in these processes remain largely unknown. The western corn rootworm (WCR, Diabrotica virgifera virgifera LeConte) (Coleoptera: Chrysomelidae) is a major corn pest that has been controlled via annual rotation between corn ( Zea mays ) and nonhost soybean ( Glycine max ) in the United States. This practice selected for a “rotation-resistant” variant (RR-WCR) with reduced ovipositional fidelity to cornfields. When in soybean fields, RR-WCRs also exhibit an elevated tolerance of antiherbivory defenses (i.e., cysteine protease inhibitors) expressed in soybean foliage. Here we show that gut bacterial microbiota is an important factor facilitating this corn specialist’s (WCR's) physiological adaptation to brief soybean herbivory. Comparisons of gut microbiota between RR- and wild-type WCR (WT-WCR) revealed concomitant shifts in bacterial community structure with host adaptation to soybean diets. Antibiotic suppression of gut bacteria significantly reduced RR-WCR tolerance of soybean herbivory to the level of WT-WCR, whereas WT-WCR were unaffected. Our findings demonstrate that gut bacteria help to facilitate rapid adaptation of insects in managed ecosystems.

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Hindgut Innate Immunity and Regulation of Fecal Microbiota through Melanization in Insects

Cited by 105 publications

References 30 publications

Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae)

Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae)

Analysis of gene expression in the midgut of Bombyx mori during the larval molting stage

Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm

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