Bacteria Associated with the Guts of Two Wood-Boring Beetles: &lt;I&gt;Anoplophora glabripennis&lt;/I&gt; and &lt;I&gt;Saperda vestita&lt;/I&gt; (Cerambycidae)

Schloss, Patrick D.; Delalibera, Ítalo; Handelsman, Jo; Raffa, Kenneth F.

doi:10.1603/0046-225x-35.3.625

Cited by 128 publications

(101 citation statements)

References 61 publications

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“…The presence of actinomycetes related to those harbored by termites was reported previously in the gut of A. glabripennis, and these bacteria may have similar aromatic degrading abilities (27).…”

Section: Discussionmentioning

confidence: 53%

Lignin degradation in wood-feeding insects

Geib

Filley

Hatcher

et al. 2008

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

298

207

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The aromatic polymer lignin protects plants from most forms of microbial attack. Despite the fact that a significant fraction of all lignocellulose degraded passes through arthropod guts, the fate of lignin in these systems is not known. Using tetramethylammonium hydroxide thermochemolysis, we show lignin degradation by two insect species, the Asian longhorned beetle (Anoplophora glabripennis) and the Pacific dampwood termite (Zootermopsis angusticollis). In both the beetle and termite, significant levels of propyl side-chain oxidation (depolymerization) and demethylation of ring methoxyl groups is detected; for the termite, ring hydroxylation is also observed. In addition, culture-independent fungal gut community analysis of A. glabripennis identified a single species of fungus in the Fusarium solani/Nectria haematococca species complex. This is a soft-rot fungus that may be contributing to wood degradation. These results transform our understanding of lignin degradation by wood-feeding insects.Asian longhorned beetle ͉ Pacific dampwood termite ͉ TMAH thermochemolysis ͉ Anoplophora glabripennis ͉ Zootermopsis angusticollis L ignin plays a central role in carbon cycling on Earth. Its heterogeneous structure imparts plants with structural rigidity and also serves to protect cellulose and hemicellulose from degradation (1). Most of what is known about lignin biodegradation is from pure culture studies with filamentous basidiomycete fungi, known as white-rot and brown-rot decay. Although both white-rot and brown-rot fungal degradation have been characterized, much more is known about the white-rot system (2, 3). White-rot fungi simultaneously degrade the three major components of the plant cell wall: lignin, cellulose, and hemicellulose. Analysis of white-rot-degraded wood shows that the reactions in lignin: (i) are oxidative, (ii) involve demethylation (or demethoxylation), (iii) include side-chain oxidation at C ␣ , and (iv) involve propyl side-chain cleavage between C ␣ and C ␤ (Fig. 1) (4). In contrast to white-rot fungi, brown-rot fungi are able to circumvent the lignin barrier, removing the hemicellulose and cellulose with only minor modification to the lignin. Consequently, lignin remains a major component of the degraded plant cell wall (5). The remaining lignin is demethylated on aryl methoxy groups and contains a greater number of ring hydroxyl groups (6).Little is known about lignin degradation in complex ecosystems, such as insect guts, where a consortium of microbes may be involved in degradation rather than just a single species. Although cellulose degradation in insect guts is well documented (7,8), the fate of lignin has not clearly been demonstrated (9, 10), and it is widely accepted that insect gut systems do not have the capacity to degrade lignin (10). Although the majority of previous reports suggest that many wood-feeding insects overcome the lignin barrier by feeding on predegraded wood (11) or through exosymbiotic relationships with wood-degrading fungi (12, 13), there are species of insects...

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Section: Discussionmentioning

confidence: 53%

Lignin degradation in wood-feeding insects

Geib

Filley

Hatcher

et al. 2008

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

298

207

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“…Chao1 index results suggest that the gut of the huhu larva harbors more than 1,800 bacterial OTUs (based on 95% lower confidence interval at 97% similarity, DNA plus RNA data set), less than the 4,500 per marine sponge (46) and more than the 100 to 500 in termite guts (based on Chao1 at 97% similarity) (21). Much less diversity (20 to 60 OTUs) has been described for cerambycid larvae (1,5,13,14,18,32,37), albeit at a coarser level of analysis.…”

Section: Discussionmentioning

confidence: 99%

“…Culture-dependent techniques have identified an abundance of Gammaproteobacteria and Actinobacteria isolates (1,5,32). Culture-independent techniques have revealed more diverse gut bacterial communities, but these are based on low (Ͻ300) numbers of clone sequences (13,15,18,37). Since the number of phylotypes detected in a sample depends strongly on the number of sequences analyzed, we generated large numbers of short sequences from 16S amplicons using pyrosequencing.…”

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confidence: 99%

Biodiversity of Active and Inactive Bacteria in the Gut Flora of Wood-Feeding Huhu Beetle Larvae (Prionoplus reticularis)

Reid

Addison

Macdonald

et al. 2011

Appl Environ Microbiol

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Huhu grubs (Prionoplus reticularis) are wood-feeding beetle larvae endemic to New Zealand and belonging to the family Cerambycidae. Compared to the wood-feeding lower termites, very little is known about the diversity and activity of microorganisms associated with xylophagous cerambycid larvae. To address this, we used pyrosequencing to evaluate the diversity of metabolically active and inactive bacteria in the huhu larval gut. Our estimate, that the gut harbors at least 1,800 phylotypes, is based on 33,420 sequences amplified from genomic DNA and reverse-transcribed RNA. Analysis of genomic DNA-and RNA-derived data sets revealed that 71% of all phylotypes (representing 95% of all sequences) were metabolically active. Rare phylotypes contributed considerably to the richness of the community and were also largely metabolically active, indicating their participation in digestive processes in the gut. The dominant families in the active community (RNA data set) included Acidobacteriaceae (24.3%), Xanthomonadaceae (16.7%), Acetobacteraceae (15.8%), Burkholderiaceae (8.7%), and Enterobacteriaceae (4.1%). The most abundant phylotype comprised 14% of the active community and affiliated with Dyella ginsengisoli (Gammaproteobacteria), suggesting that a Dyella-related organism is a likely symbiont. This study provides new information on the diversity and activity of gutassociated microorganisms that are essential for the digestion of the nutritionally poor diet consumed by wood-feeding larvae. Many huhu gut phylotypes affiliated with insect symbionts or with bacteria present in acidic environments or associated with fungi.

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“…Initially, this work was focused on the genetic manipulation of insect symbionts to block the transmission of pathogens vectored by insects (4). This approach has since widened to target insect pests directly (12,17,22,25). As a first step toward the development of such an approach with Australian scarab pests, we have characterized a subset of the bacterial community that naturally associates with the scarab hindgut, in order to identify potential candidates for genetic manipulation strategies targeting the feeding activity of these beetles.…”

mentioning

confidence: 99%

“Endomicrobia” and Other Bacteria Associated with the Hindgut ofDermolepida albohirtumLarvae

Pittman¹,

Brumbley

Allsopp³

et al. 2008

Appl Environ Microbiol

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Symbiotic bacteria residing in the hindgut chambers of scarab beetle larvae may be useful in paratransgenic approaches to reduce larval root-feeding activities on agricultural crops. We compared the bacterial community profiles associated with the hindgut walls of individual Dermolepida albohirtum third-instar larvae over 2 years and those associated with their plant root food source among different geographic regions. Denaturing gradient gel electrophoresis analysis was used with universal and Actinobacteria-specific 16S rRNA primers to reveal a number of taxa that were found consistently in all D. albohirtum larvae but not in samples from their food source, sugarcane roots. These taxa included representatives from the "Endomicrobia," Firmicutes, Proteobacteria, and Actinobacteria and were related to previously described bacteria from the intestines of other scarab larvae and termites. These universally distributed taxa have the potential to form vertically transmitted symbiotic associations with these insects.There has been growing research interest in developing novel approaches to manage insect pests and the pathogens they transmit through the genetic manipulation of microorganisms that intimately associate with these insects (3,19). Initially, this work was focused on the genetic manipulation of insect symbionts to block the transmission of pathogens vectored by insects (4). This approach has since widened to target insect pests directly (12,17,22,25). As a first step toward the development of such an approach with Australian scarab pests, we have characterized a subset of the bacterial community that naturally associates with the scarab hindgut, in order to identify potential candidates for genetic manipulation strategies targeting the feeding activity of these beetles.The hindgut chambers of scarab larvae are known to house dense microbial communities that participate in the fermentation of plant material (1, 13). Molecular characterization of the bacterial communities in the midguts, hindguts, and food sources of humivorous larvae of the East African scarab Pachnoda ephippiata showed significant differences across all three environments (6), although some gut taxa matched close relatives found in rhizosphere communities, suggesting that transient associations occur in the larval gut environment. However, in the case of root-feeding larvae of the European cockchafer Melolontha melolontha, terminal restriction fragment length polymorphism profiles compared across regions revealed a diverse and consistent bacterial community on the hindgut walls of larvae (5). Many of the taxa were related to gut bacteria identified in other beetles, termites, and the vertebrate rumen, suggesting a specific and functional role in cellulose digestion.In Australia, scarab beetles are major pests in sugarcane production through the feeding damage that larvae cause to plant root systems. Nineteen species of endemic melolonthine beetles cause significant damage to Australian sugarcane (14).The most important species is Dermolepi...

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Bacteria Associated with the Guts of Two Wood-Boring Beetles: <I>Anoplophora glabripennis</I> and <I>Saperda vestita</I> (Cerambycidae)

Cited by 128 publications

References 61 publications

Lignin degradation in wood-feeding insects

Lignin degradation in wood-feeding insects

Biodiversity of Active and Inactive Bacteria in the Gut Flora of Wood-Feeding Huhu Beetle Larvae (Prionoplus reticularis)

“Endomicrobia” and Other Bacteria Associated with the Hindgut ofDermolepida albohirtumLarvae

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