Gut microbiota degrades toxic isothiocyanates in a flea beetle pest

Shukla, Shantanu; Beran, Franziska

doi:10.1111/mec.15657

Cited by 60 publications

(63 citation statements)

References 83 publications

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“…However, instead of the isothiocyanate, we detected mainly the nitrile hydrolysis product of 4MSOB glucosinolate in P. armoraciae bodies and feces ( Figure 2B ). There are several possible explanations for this unexpected result: 4MSOB isothiocyanate may not have been recovered completely with our extraction methods because it has reacted with proteins or has been metabolized by the beetle or associated gut microbes ( Brown and Hampton, 2011 ; Jeschke et al, 2015 ; van den Bosch and Welte, 2017 ; Friedrichs et al, 2020 ; Shukla and Beran, 2020 ). Alternatively, P. armoraciae may be able to manipulate the outcome of glucosinolate hydrolysis and promote the formation of the less reactive nitrile instead of the isothiocyanate.…”

Section: Discussionmentioning

confidence: 99%

Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

et al. 2021

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Myrosinase enzymes play a key role in the chemical defense of plants of the order Brassicales. Upon herbivory, myrosinases hydrolyze the β-S-linked glucose moiety of glucosinolates, the characteristic secondary metabolites of brassicaceous plants, which leads to the formation of different toxic hydrolysis products. The specialist flea beetle, Phyllotreta armoraciae, is capable of accumulating high levels of glucosinolates in the body and can thus at least partially avoid plant myrosinase activity. In feeding experiments with the myrosinase-deficient Arabidopsis thaliana tgg1 × tgg2 (tgg) mutant and the corresponding Arabidopsis Col-0 wild type, we investigated the influence of plant myrosinase activity on the metabolic fate of ingested glucosinolates in adult P. armoraciae beetles. Arabidopsis myrosinases hydrolyzed a fraction of ingested glucosinolates and thereby reduced the glucosinolate sequestration rate by up to 50% in adult beetles. These results show that P. armoraciae cannot fully prevent glucosinolate hydrolysis; however, the exposure of adult beetles to glucosinolate hydrolysis products had no impact on the beetle’s energy budget under our experimental conditions. To understand how P. armoraciae can partially prevent glucosinolate hydrolysis, we analyzed the short-term fate of ingested glucosinolates and found them to be rapidly absorbed from the gut. In addition, we determined the fate of ingested Arabidopsis myrosinase enzymes in P. armoraciae. Although we detected Arabidopsis myrosinase protein in the feces, we found only traces of myrosinase activity, suggesting that P. armoraciae can inactivate plant myrosinases in the gut. Based on our findings, we propose that the ability to tolerate plant myrosinase activity and a fast glucosinolate uptake mechanism represent key adaptations of P. armoraciae to their brassicaceous host plants.

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Section: Discussionmentioning

confidence: 99%

Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

et al. 2021

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“…For example, some insect species possess a gut microbiota mainly constituted by stable, resident microbiota, as occurs with the American cockroach or B. tryoni ( Tinker and Ottesen, 2016 ; Majumder et al, 2019 ). Other species have a much less stable gut microbiota mainly conformed by transient microbiota, as has been documented in larval or adult butterflies ( Hammer et al, 2017 ; Phalnikar et al, 2019 ; Ravenscraft et al, 2019a , b ), the giant neotropical bullet ant, Paraponera clavata or other rainforest ants ( Sanders et al, 2017 ), Drosophila melanogaster or other species within Drosophila ( Wong et al, 2013 ; Hammer et al, 2017 , 2019 ; Moreau and Rubin, 2017 ; Ma and Leulier, 2018 ; Ross et al, 2018 ; Phalnikar et al, 2019 ), the cabbage stem flea beetle Psylliodes chrysocephala ( Shukla and Beran, 2020 ) or other beetles ( Kelley and Dobler, 2011 ), hard ticks ( Guizzo et al, 2020 ), dragonflies ( Deb et al, 2019 ), and mosquitoes ( Coon et al, 2016 ), but this phenomenon had not been documented previously in the highly polyphagous and pestiferous A . ludens or any other Anastrepha species.…”

Section: Discussionmentioning

confidence: 99%

“…In general, there seems to be a consensus indicating that the transient microbiota plays no significant role on the insect’s physiology ( Hammer et al, 2017 ), though notable exceptions exist ( Kikuchi et al, 2007 ; Coon et al, 2016 ; Heys et al, 2018 ; Ross et al, 2018 ). Sometimes the acquisition of microbes from the environment can provide symbionts with functions that are uniquely relevant, including the ability to digest the food which the microbes originally came from Ravenscraft et al (2019a) and Shukla and Beran (2020) .…”

Section: Discussionmentioning

confidence: 99%

Metagenomic Survey of the Highly Polyphagous Anastrepha ludens Developing in Ancestral and Exotic Hosts Reveals the Lack of a Stable Microbiota in Larvae and the Strong Influence of Metamorphosis on Adult Gut Microbiota

et al. 2021

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We studied the microbiota of a highly polyphagous insect, Anastrepha ludens (Diptera: Tephritidae), developing in six of its hosts, including two ancestral (Casimiroa edulis and C. greggii), three exotic (Mangifera indica cv. Ataulfo, Prunus persica cv. Criollo, and Citrus x aurantium) and one occasional host (Capsicum pubescens cv. Manzano), that is only used when extreme drought conditions limit fruiting by the common hosts. One of the exotic hosts (“criollo” peach) is rife with polyphenols and the occasional host with capsaicinoids exerting high fitness costs on the larvae. We pursued the following questions: (1) How is the microbial composition of the larval food related to the composition of the larval and adult microbiota, and what does this tell us about transience and stability of this species’ gut microbiota? (2) How does metamorphosis affect the adult microbiota? We surveyed the microbiota of the pulp of each host fruit, as well as the gut microbiota of larvae and adult flies and found that the gut of A. ludens larvae lacks a stable microbiota, since it was invariably associated with the composition of the pulp microbiota of the host plant species studied and was also different from the microbiota of adult flies indicating that metamorphosis filters out much of the microbiota present in larvae. The microbiota of adult males and females was similar between them, independent of host plant and was dominated by bacteria within the Enterobacteriaceae. We found that in the case of the “toxic” occasional host C. pubescens the microbiota is enriched in potentially deleterious genera that were much less abundant in the other hosts. In contrast, the pulp of the ancestral host C. edulis is enriched in several bacterial groups that can be beneficial for larval development. We also report for the first time the presence of bacteria within the Arcobacteraceae family in the gut microbiota of A. ludens stemming from C. edulis. Based on our findings, we conclude that changes in the food-associated microbiota dictate major changes in the larval microbiota, suggesting that most larval gut microbiota is originated from the food.

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“…However, we detected much more 4MSOB cyanide in P. armoraciae bodies and feces relative to 4MSOB isothiocyanate and its derivatives (Figure 1B). There are several possible explanations for this unexpected result: 4MSOB isothiocyanate may not have been recovered completely with our extraction methods because it reacted with proteins or was metabolized by the beetle or associated gut microbes (Brown and Hampton, 2011; Jeschke et al, 2015; van den Bosch and Welte, 2017; Friedrichs et al, 2020; Shukla and Beran, 2020). Alternatively, P. armoraciae may be able to manipulate the outcome of glucosinolate hydrolysis and promote the formation of less toxic 4MSOB cyanide instead of 4MSOB isothiocyanate.…”

Section: Discussionmentioning

confidence: 98%

A specialist flea beetle manipulates and tolerates the activated chemical defense in its host plant

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Körnig

Wielsch

et al. 2021

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Glucosinolates, the characteristic secondary metabolites of Brassicales, are hydrolyzed upon herbivory by myrosinases to toxic and deterrent defense metabolites. The specialist flea beetle, Phyllotreta armoraciae, sequesters glucosinolates in the body despite myrosinase activity, but it is unknown whether plant myrosinase activity influences sequestration and how beetles prevent the hydrolysis of ingested glucosinolates. In feeding experiments performed with the myrosinase-deficient Arabidopsis thaliana tgg1tgg2 (tgg) mutant and the corresponding wild type, we found that plant myrosinases reduced the glucosinolate sequestration rate by up to 50% and hydrolyzed a fraction of ingested glucosinolates in adult beetles. Although these results show that P. armoraciae cannot fully prevent glucosinolate hydrolysis, we observed no negative influence on beetle performance. To understand how P. armoraciae can avoid the hydrolysis of some ingested glucosinolates, we analyzed their fate directly after ingestion. P. armoraciae rapidly absorbed glucosinolates across the gut epithelium, a strategy that has been proposed to prevent hydrolysis in the gut lumen of sequestering insects. Moreover, beetle gut content suppressed in vitro myrosinase activity, and almost no myrosinase activity was detectable in the feces, which indicates that ingested myrosinases are inactivated in the beetle gut. In summary, we show that P. armoraciae uses several strategies to prevent the hydrolysis of ingested glucosinolates but can also tolerate the formation of glucosinolate hydrolysis products.

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Gut microbiota degrades toxic isothiocyanates in a flea beetle pest

Cited by 60 publications

References 83 publications

Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

Metagenomic Survey of the Highly Polyphagous Anastrepha ludens Developing in Ancestral and Exotic Hosts Reveals the Lack of a Stable Microbiota in Larvae and the Strong Influence of Metamorphosis on Adult Gut Microbiota

A specialist flea beetle manipulates and tolerates the activated chemical defense in its host plant

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