Gut Microbes Contribute to Nitrogen Provisioning in a Wood-Feeding Cerambycid

Ayayee, Paul A.; Rosa, Cristina; Ferry, James G.; Felton, Gary W.; Saunders, Michael C.; Hoover, Kelli

doi:10.1603/en14045

Cited by 59 publications

(67 citation statements)

References 44 publications

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“…Microbes in the gut of A. glabripennis are known to have definitive roles in nutrient biosynthesis and nutrient recycling, helping the beetle to thrive under nutrient-poor conditions [35, 42, 43]. A. glabripennis microbes encode an arsenal of laccases, peroxidases, aldo-keto reductases, dyp-type peroxidases [30], and at least one lignin peroxidase, which is encoded by a fungal symbiont belonging to the F. solani species complex [44].…”

Section: Resultsmentioning

confidence: 99%

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

et al. 2016

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BackgroundRelatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.ResultsThe Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.ConclusionsAmplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

et al. 2016

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“…Gut microbiota are ubiquitous for insect herbivores and are often critical to insect biological performance and ecological functioning, such as augmentation of nutritional availability [1,2,3], protection of insects from pathogens and parasites [4,5], facilitation of pheromone production [6,7], and detoxification of harmful toxins produced by the host plant defense system [8,9]. The gut microbiome has also been recognized as a major force in shaping insect-plant interactions [10,11,12].…”

Section: Introductionmentioning

confidence: 99%

Pine Defensive Monoterpene α-Pinene Influences the Feeding Behavior of Dendroctonus valens and Its Gut Bacterial Community Structure

Shi

Wang

et al. 2016

IJMS

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The exposure to plant defense chemicals has negative effects on insect feeding activity and modifies insect gut microbial community composition. Dendroctonus valens is a very destructive forest pest in China, and harbors a large diversity and abundance of gut microorganisms. Host pine defensive chemicals can protect the pines from attack by the holobiont. In this study, boring length of D. valens feeding on 0 mg/g α-pinene and 9 mg/g α-pinene concentration in phloem media for 6 and 48 h were recorded, and their gut bacterial communities were analyzed in parallel. Nine milligram per gram α-pinene concentration significantly inhibited boring length of D. valens and altered its gut microbial community structure after 6 h. The inhibition of boring length from 9 mg/g α-pinene in diets ceased after 48 h. No significant differences of the bacterial communities were observed between the beetles in 0 and 9 mg/g α-pinene concentration in phloem media after 48 h. Our results showed that the inhibition of the feeding behavior of D. valens and the disturbance to its gut bacterial communities in 9 mg/g α-pinene concentration in phloem media after 6 h were eliminated after 48 h. The resilience of gut bacterial community of D. valens may help the beetle catabolize pine defense chemical.

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“…; Ayayee et al. ) and wood‐inhabiting fungi that grow in the phloem and sapwood (Bleiker and Six ; Cook et al. ; Six et al.…”

Section: Discussionmentioning

confidence: 99%

“…In part this shortage of essential amino acids has been alleviated by the evolution of obligate symbiosis with nitrogen-fixing and nitrogen-recycling bacteria in the gut of larvae (Morales-Jimenez et al 2013;Ayayee et al 2014) and wood-inhabiting fungi that grow in the phloem and sapwood (Bleiker and Six 2007;Cook et al 2010;Six et al 2011). Both adaptations supplement the amount of nitrogen in the diets of larval beetles by as much as 40%, thus enhancing their survival and growth.…”

Section: Discussionmentioning

confidence: 99%

Are outbreaks of cambium‐feeding beetles generated by nutritionally enhanced phloem of drought‐stressed trees?

White

2014

J Applied Entomology

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Outbreaks of cambium-feeding beetles follow droughts, becoming most severe in overmature trees and those growing on stressful sites or planted beyond their natural range. Outbreaks develop from small endemic populations confined to a few senescing or damaged trees and expand into neighbouring trees that become newly stressed as a drought intensifies, eventually coalescing as a full-blown outbreak. The beetles' larvae normally face a severe nutritional challenge feeding on the slow outflow of dilute nutrients in the phloem of damaged or senescing trees. This is reflected in their slow rate of growth. But when drought stresses trees, they senesce more quickly, releasing a faster flow of more concentrated nutrients that enhances the survival of the insects. The increased survival and faster rate of growth of larvae feeding in this enriched phloem can generate an outbreak. Both the dieback of the trees and the outbreaks of these insects are generated by drought. This hypothesis presents a parsimonious explanation for outbreaks of cambium-feeding insects. Apart from providing a focus for future research, it has the added benefit that it replaces non-explanatory descriptions of these outbreaks with a testable biological explanation based on known plant and insect physiology.

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Gut Microbes Contribute to Nitrogen Provisioning in a Wood-Feeding Cerambycid

Cited by 59 publications

References 44 publications

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface

Pine Defensive Monoterpene α-Pinene Influences the Feeding Behavior of Dendroctonus valens and Its Gut Bacterial Community Structure

Are outbreaks of cambium‐feeding beetles generated by nutritionally enhanced phloem of drought‐stressed trees?

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