eThe mountain pine beetle, Dendroctonus ponderosae, is a subcortical herbivore native to western North America that can kill healthy conifers by overcoming host tree defenses, which consist largely of high terpene concentrations. The mechanisms by which these beetles contend with toxic compounds are not well understood. Here, we explore a component of the hypothesis that beetle-associated bacterial symbionts contribute to the ability of D. ponderosae to overcome tree defenses by assisting with terpene detoxification. Such symbionts may facilitate host tree transitions during range expansions currently being driven by climate change. For example, this insect has recently breached the historical geophysical barrier of the Canadian Rocky Mountains, providing access to näive tree hosts and unprecedented connectivity to eastern forests. We use culture-independent techniques to describe the bacterial community associated with D. ponderosae beetles and their galleries from their historical host, Pinus contorta, and their more recent host, hybrid P. contorta-Pinus banksiana. We show that these communities are enriched with genes involved in terpene degradation compared with other plant biomass-processing microbial communities. These pine beetle microbial communities are dominated by members of the genera Pseudomonas, Rahnella, Serratia, and Burkholderia, and the majority of genes involved in terpene degradation belong to these genera. Our work provides the first metagenome of bacterial communities associated with a bark beetle and is consistent with a potential microbial contribution to detoxification of tree defenses needed to survive the subcortical environment.
Sirex noctilio is an invasive wood-feeding wasp that threatens the world's commercial and natural pine forests. Successful tree colonization by this insect is contingent on the decline of host defenses and the ability to utilize the woody substrate as a source of energy. We explored its potential association with bacterial symbionts that may assist in nutrient acquisition via plant biomass deconstruction using growth assays, culture-dependent and -independent analysis of bacterial frequency of association and whole-genome analysis. We identified Streptomyces and c-Proteobacteria that were each associated with 94% and 88% of wasps, respectively. Streptomyces isolates grew on all three cellulose substrates tested and across a range of pH 5.6 to 9. On the basis of whole-genome sequencing, three Streptomyces isolates have some of the highest proportions of genes predicted to encode for carbohydrate-active enzymes (CAZyme) of sequenced Actinobacteria. c-Proteobacteria isolates grew on a cellulose derivative and a structurally diverse substrate, ammonia fiber explosion-treated corn stover, but not on microcrystalline cellulose. Analysis of the genome of a Pantoea isolate detected genes putatively encoding for CAZymes, the majority predicted to be active on hemicellulose and more simple sugars. We propose that a consortium of microorganisms, including the described bacteria and the fungal symbiont Amylostereum areolatum, has complementary functions for degrading woody substrates and that such degradation may assist in nutrient acquisition by S. noctilio, thus contributing to its ability to be established in forested habitats worldwide.
Bacterial communities are known to play important roles in insect life histories, yet their consistency or variation across populations is poorly understood. Bacteria associated with the bark beetle Dendroctonus valens LeConte from eight populations, ranging from Wisconsin to Oregon, were evaluated and compared. We used the culture-independent technique of denaturing gradient gel electrophoresis to visualize bacterial diversity, or individual operational taxonomic units (OTUs), from individual beetles. One-way analysis of similarities was used to test for differences of bacterial communities between sites. Analysis of community profiles showed that individual beetles on average contained 10 OTUs, with frequency of association from 2 to 100% of beetles. OTU sequences most closely matched beta- and gamma-proteobacteria, and one each matched Bacilli and Actinobacteria. Several OTUs were particularly abundant, most notably an Actinobacterium from 100% and two Proteobacteria from 60% of beetles sampled. Some OTUs were similar to previously described bacteria with known biochemical capabilities and ecological functions, suggesting that some bacterial associates of D. valens may contribute to its ability to exploit a resource low in nutrients and high in defensive compounds. There were significant differences of bacterial communities between sites. The strength of these differences was positively correlated with distance between sites, although additional unexplained factors also contribute to the variation.
Multi-trophic interactions between prokaryotes, unicellular eukaryotes, and ecologically intertwined metazoans are presumably common in nature, yet rarely described. The mountain pine beetle, Dendroctonus ponderosae, is associated with two filamentous fungi, Grosmannia clavigera and Ophiostoma montium. Other microbes, including yeasts and bacteria, are also present in the phloem, but it is not known whether they interact with the symbiotic fungi or the host beetle. To test whether such interactions occur, we performed a suite of in vitro assays. Overall, relative yield of O. montium grown with microbes isolated from larval galleries was significantly greater than when the fungus was grown alone. Conversely, the yield of G. clavigera grown with these same microbes was less than or equal to when it was grown alone, suggesting that O. montium, and at least some microbes in larval galleries, have a mutualistic or commensal relationship, while G. clavigera and those same microbes have an antagonistic relationship. A bacterium isolated from phloem not colonized by beetles was found to inhibit growth of both G. clavigera and O. montium and appears to be an antagonist to both fungi. Our results suggest that bacteria and yeasts likely influence the distribution of mycangial fungi in the host tree, which, in turn, may affect the fitness of D. ponderosae.
Streptomyces sp. strain Wigar10 was isolated from a surface-sterilized garlic bulb (Allium sativum var. Purple Stripe). Its genome encodes several novel secondary metabolite biosynthetic gene clusters and provides a genetic basis for further investigation of this strain's chemical biology and potential for interaction with its garlic host.Garlic has a long history as a medicinal herb, with wellknown bioactivities, including antimicrobial, antifungal, and antiparasitic properties (1). We isolated actinobacteria from garlic to begin exploring their potential contribution to its chemical ecology. Bulbs of Allium sativum var. Purple Stripe were surface sterilized by sequential submersion in ethanol and phosphate-buffered saline for 10 s each, repeated in triplicate, and then masticated using a minipestle in a 2-ml microcentrifuge tube. Actinobacteria were isolated by plating 100 l of the extract onto chitin-agar plates supplemented with nystatin (21.3 ml/liter of a 2-mg/ml stock in dimethyl sulfoxide) that were incubated at 25°C for at least 4 weeks. One isolate, strain Wigar10, produced large zones of clearing in preliminary plate bioassays against Trichoderma harzianum, Fusarium oxysporum, and Aspergillus niger, leading to its selection for genome sequencing.Wigar10 genomic DNA was extracted according to the methods described by Graff and Conrad (3) and sequenced at the DOE Joint Genome Institute (JGI). Shotgun Titanium 454 sequencing (1/4 plate; Roche) yielded 96.9 Mbp of sequence, which was assembled using Newbler (Roche) into 721 contigs of Ͼ350 bp (maximum, 90,402 bp) comprising 8,178,919 bp in total (i.e., 11.8ϫ coverage). The overall GϩC content and coding density were 71.9% and 84.1%, respectively. Using Prodigal (5) according to default parameters, 8,315 complete and 1,020 truncated reading frames were predicted, which were functionally annotated using the COG (11) and Pfam (2) databases. Single 5S and 16S rRNA genes were annotated using RNAmer (7). tRNAscan-SE (8) annotated 60 tRNA genes representing all 20 amino acids. Strain Wigar10 belongs to the genus Streptomyces, having a 16S rRNA gene most related (99.9% over 1,365 positions) to S. roseochromogenus NBRC3442, S. cavourensis subsp. cavourensis NBRC13026, and S. globisporus subsp. globisprous NBRC12208 (GenBank accession numbers AB184777, AB184264, and AB184066, respectively). Its genome has higher average amino acid identities (84.2 and 84.1%, respectively) than S. griseus subsp. griseus NBRC13350 (10) and S. griseus strain XylebKG-1 (4); amino acid identities were calculated according to the method described by Konstantinidis and Tiedje (6).Secondary metabolite biosynthetic gene clusters encoded by Streptomyces sp. Wigar10 were predicted using antiSMASH v1.1.0 (9). Homologous clusters found in either S. griseus subsp. griseus NBRC13350 or S. griseus strain XylebKG-1 are predicted to encode a LuxA/C-type siderophore, carotenoids, hopanes, geosmin, ectoine, melanin, A-factor, the nonribosomal peptide synthetase (NPRS)-produced siderophore griseobactin...
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