An IMD-like pathway mediates the intestinal immunity to modulate the homeostasis of gut microbiota in Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

Xiao, Rong; Wang, Xinghong; Xie, Erming; Ji, Tianliang; Li, Xiongwei; Muhammad, Aliyu Idris; Yin, Xianyuan; Hou, Youming; Shi, Zhanghong

doi:10.1016/j.dci.2019.03.013

Cited by 25 publications

(25 citation statements)

References 37 publications

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“…Silencing the expression of Relish in the model insect G. mellonella results in a significant increase in the concentration of gut bacteria and decreases in the expression of AMPs [ 68 ]. Similar findings were also reported in Red palm weevil, which showed a compromised ability of pathogen clearance and increased gut bacterial load after silencing the Relish expression [ 69 ]. Moreover, a change in the gut commensal microbiota was observed after the inhibition of Caudal, a transcription repressor of NF-κB-mediated expression of AMPs [ 70 ].…”

Section: The Interaction Between Host Immunity and Gut Microbiotasupporting

confidence: 85%

The Tripartite Interaction of Host Immunity–Bacillus thuringiensis Infection–Gut Microbiota

Mandal

et al. 2020

Toxins

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Bacillus thuringiensis (Bt) is an important cosmopolitan bacterial entomopathogen, which produces various protein toxins that have been expressed in transgenic crops. The evolved molecular interaction between the insect immune system and gut microbiota is changed during the Bt infection process. The host immune response, such as the expression of induced antimicrobial peptides (AMPs), the melanization response, and the production of reactive oxygen species (ROS), varies with different doses of Bt infection. Moreover, B. thuringiensis infection changes the abundance and structural composition of the intestinal bacteria community. The activated immune response, together with dysbiosis of the gut microbiota, also has an important effect on Bt pathogenicity and insect resistance to Bt. In this review, we attempt to clarify this tripartite interaction of host immunity, Bt infection, and gut microbiota, especially the important role of key immune regulators and symbiotic bacteria in the Bt killing activity. Increasing the effectiveness of biocontrol agents by interfering with insect resistance and controlling symbiotic bacteria can be important steps for the successful application of microbial biopesticides.

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Section: The Interaction Between Host Immunity and Gut Microbiotasupporting

confidence: 85%

The Tripartite Interaction of Host Immunity–Bacillus thuringiensis Infection–Gut Microbiota

Mandal

et al. 2020

Toxins

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“…Experimental evidence for screening is so far limited in insect-microbe associations (Innocent et al, 2018, Itoh et al, 2019, Ranger et al, 2018), but the results of our study provide support for the prediction that screening is more likely to evolve if a host’s challenging environment is derived from defence traits against parasites (Archetti et al, 2011a, Archetti et al, 2011b). Altogether, our study provides evidence that the well-established cross talk between the immune system and gut associated microbes in vertebrates and invertebrates (Chu and Mazmanian, 2013, Rakoff-Nahoum et al, 2004, Slack et al, 2009, Watnick and Jugder, 2020, Xiao et al, 2019) holds for a broader range of immune defence traits ( sensu Otti et al, 2014) and might be realized not only through signalling but also screening.…”

Section: Resultsmentioning

confidence: 57%

“…Generally, the immune system together with physiochemical properties of the gut environment maintains the homeostasis between gut associated microbes and the host (Chu and Mazmanian, 2013, McFall-Ngai et al, 2013, Rakoff-Nahoum et al, 2004, Slack et al, 2009, Watnick and Jugder, 2020, Xiao et al, 2019, see also Foster et al, 2017). Highly acidic stomach lumens are ubiquitous in higher vertebrates, including amphibians, reptiles, birds and mammals (Beasley et al, 2015, Koelz, 1992), while in insects, acidic regions have rarely been described so far from midgut regions (Chapman, 2013, Holtof et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Tragust

Herrmann

Häfner

et al. 2020

Preprint

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12Animals continuously encounter microorganisms that are essential for health or cause disease. 13 They are thus challenged to control harmful microbes while allowing acquisition of beneficial 14 microbes, a challenge that is likely especially important concerning microbes in food and in 15 animals such as social insects that exchange food among colony members. Here we show that 16 formicine ants actively swallow their antimicrobial, highly acidic poison gland secretions 17 after feeding. The ensuing creation of an acidic environment in the stomach, the crop, 18 improves individual survival in the face of pathogen contaminated food and limits disease 19 transmission during mutual food exchange. At the same time, crop acidification selectively 20 allows acquisition and colonization by known bacterial gut associates. The results of our 21 study suggest that swallowing of acidic poison gland secretions acts as a microbial filter in 22 formicine ants and indicate a potentially widespread but so far underappreciated dual role of 23 antimicrobials in host-microbe interactions. 24 25 85 5 experimental manipulation of poison gland access, and behavioural observations. In loss of 86 poison gland function experiments, we then investigate whether analogous to acidic stomachs 87 of higher vertebrates and acidic midgut regions in the fruit fly, swallowing of poison gland 88 substances can serve gut microbial control and prevent bacterial pathogen infection and 89 transmission. Finally, we explore whether swallowing of poison gland substances acts as a 90 microbial filter that is permissible to gut colonization of bacteria from the family 91 Acetobacteracea. 92 93 Results and Discussion 94To reveal whether poison gland secretions are swallowed during acidopore grooming, we 95 monitored acidity levels in the crop lumen of the Florida carpenter ant Camponotus floridanus 96 at different time points after feeding them 10% honey water (pH = 5). We found that over 97 time, the crop lumen became increasingly acidic, reaching highly acidic values 48h after 98 feeding (median pH = 2; 95% CI: 1.5-3.4), whilst renewed access to food after 48h restored 99 the pH to levels recorded after the first feeding trial ( Fig. 1a; LMM, LR-test, χ 2 = 315.18, df = 100 3, P < 0.001; Westfall corrected post-hoc comparisons: 0+4h vs. 48h+4h: P = 0.317, all other 101 comparisons: P < 0.001). This acidification was limited to the crop and did not extend to the 102 midgut (Fig. 1figure supplement 1; pH-measurements at four points along the midgut 24h 103 after access to 10% honey-water; mean ± se; midgut position 1 = 5.08 ± 0.18, midgut position 104 2 = 5.28 ± 0.17, midgut position 3 = 5.43 ± 0.16, midgut position 4 = 5.31 ± 0.19). Prevention 105 of acidopore grooming in C. floridanus ants for 24h after feeding resulted in a significantly 106 diminished acidification of the crop lumen (Fig. 1b; LMM, LR-test, χ 2 = 44.68, df = 1, P < 107 0.001), a result that was invariably obtained in a comparative survey across seven formicine 108 ant species (g...

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“…The red palm weevil Rhynchophorus ferrugineus (Coleoptera: Curculionidae) is a devastating pest, which has been spread to various regions with palm trees in southern China, causing serious damage to the palm industry and landscape (Hou et al, 2011;Wang et al, 2015Wang et al, , 2017Muhammad et al, 2017;Ali et al, 2018). Red palm weevil larvae have a long life span, strong ability to drill collar, and strong adaptability to different environments (Shi et al, 2014;Peng et al, 2016;Dawadi et al, 2018;Habineza et al, 2019;Xiao et al, 2019). Due to damage to vascular tissues and consumption of large amounts of crown tissues, red palm weevil larvae can cause the death of palm trees (Butera et al, 2012;Muhammad et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Neuropeptides and G-Protein Coupled Receptors (GPCRs) in the Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

et al. 2020

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The red palm weevil Rhynchophorus ferrugineus is a devastating, invasive pest that causes serious damages to palm trees, and its invasiveness depends on its strong ability of physiological and behavioral adaptability. Neuropeptides and their receptors regulate physiology and behavior of insects, but these protein partners have not been identified from many insects. Here, we systematically identified neuropeptide precursors and the corresponding receptors in the red palm weevil, and analyzed their tissue expression patterns under control conditions and after pathogen infection. A total of 43 putative neuropeptide precursors were identified, including an extra myosuppressin peptide was identified with amino acid substitutions at two conserved sites. Forty-four putative neuropeptide receptors belonging to three classes were also identified, in which neuropeptide F receptors and insulin receptors were expanded compared to those in other insects. Based on qRT-PCR analyses, genes coding for several neuropeptide precursors and receptors were highly expressed in tissues other than the nervous system, suggesting that these neuropeptides and receptors play other roles in addition to neuro-reception. Some of the neuropeptides and receptors, like the tachykininrelated peptide and receptor, were significantly induced by pathogen infection, especially sensitive to Bacillus thuringiensis and Metarhizium anisopliae. Systemic identification and initial characterization of neuropeptides and their receptors in the red palm weevil provide a framework for further studies to reveal the functions of these ligand-and receptor-couples in regulating physiology, behavior, and immunity in this important insect pest species.

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An IMD-like pathway mediates the intestinal immunity to modulate the homeostasis of gut microbiota in Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

Cited by 25 publications

References 37 publications

The Tripartite Interaction of Host Immunity–Bacillus thuringiensis Infection–Gut Microbiota

The Tripartite Interaction of Host Immunity–Bacillus thuringiensis Infection–Gut Microbiota

Formicine ants swallow their highly acidic poison for gut microbial selection and control

Neuropeptides and G-Protein Coupled Receptors (GPCRs) in the Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

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