Detection and characterization of bacterial symbionts in the Heteropteran,<i>Blissus insularis</i>

Boucias, Drion G.; Garcia-Maruniak, Alejandra; Cherry, Ron; Lu, Huangjun; Maruniak, James E.; Lietze, Verena-Ulrike

doi:10.1111/j.1574-6941.2012.01433.x

Cited by 42 publications

(99 citation statements)

References 46 publications

(63 reference statements)

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“…For some insects, resistance has been attributed to the production of antimicrobial cuticular compounds (53)(54)(55). More recently there is growing evidence that some of these compounds are not produced by the insects themselves but by endogenous microbial flora, adding an interesting twist to coevolutionary scenarios (56,57). In other insects, specific behaviors, including heat seeking (behavioral fever), aggregation, and, in the case of social insects, grooming, have also been shown to be strategies for impeding or minimizing microbial infections (58)(59)(60).…”

Section: Discussionmentioning

confidence: 99%

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Pedrini

Ortiz‐Urquiza

Huarte‐Bonnet

et al. 2015

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

123

118

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Entomopathogenic fungi and their insect hosts represent a model system for examining invertebrate-pathogen coevolutionary selection processes. Here we report the characterization of competing components of an arms race consisting of insect protective antimicrobial compounds and evolving fungal mechanisms of detoxification. The insect pathogenic fungus Beauveria bassiana has a remarkably wide host range; however, some insects are resistant to fungal infection. Among resistant insects is the tenebrionid beetle Tribolium castaneum that produces benzoquinone-containing defensive secretions. Reduced fungal germination and growth was seen in media containing T. castaneum dichloromethane extracts or synthetic benzoquinone. In response to benzoquinone exposure, the fungus expresses a 1,4-benzoquinone oxidoreductase, BbbqrA, induced >40-fold. Gene knockout mutants (ΔBbbqrA) showed increased growth inhibition, whereas B. bassiana overexpressing BbbqrA (Bb::BbbqrAO) displayed increased resistance to benzoquinone compared with wild type. Increased benzoquinone reductase activity was detected in wild-type cells exposed to benzoquinone and in the overexpression strain. Heterologous expression and purification of BbBqrA in Escherichia coli confirmed NAD(P)H-dependent benzoquinone reductase activity. The ΔBbbqrA strain showed decreased virulence toward T. castaneum, whereas overexpression of BbbqrA increased mortality versus T. castaneum. No change in virulence was seen for the ΔBbbqrA or Bb::BbbqrAO strains when tested against the greater wax moth Galleria mellonella or the beetle Sitophilus oryzae, neither of which produce significant amounts of cuticular quinones. The observation that artificial overexpression of BbbqrA results in increased virulence only toward quinone-secreting insects implies the lack of strong selection or current failure of B. bassiana to counteradapt to this particular host defense throughout evolution.

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Section: Discussionmentioning

confidence: 99%

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Pedrini

Ortiz‐Urquiza

Huarte‐Bonnet

et al. 2015

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

123

118

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“…This insect, a primary pest of St. Augustinegrass, Stenotaphrum secundatum (Walter) Kuntze (20,21), feeds on the grass phloem, resulting in diminished grass growth, yellowing and brown blade color, and the eventual death of grass patches (22,23). Investigations of multiple B. insularis field populations demonstrated that complex Burkholderia ribotypes were present within and among the populations (12). The copy number of the Burkholderia 16S rRNA gene increased with the age of B. insularis insects, and antibiotic treatment reduced Burkholderia numbers and slowed B. insularis development, pointing to a mutualistic Blissus-Burkholderia association (12).…”

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confidence: 99%

“…Investigations of multiple B. insularis field populations demonstrated that complex Burkholderia ribotypes were present within and among the populations (12). The copy number of the Burkholderia 16S rRNA gene increased with the age of B. insularis insects, and antibiotic treatment reduced Burkholderia numbers and slowed B. insularis development, pointing to a mutualistic Blissus-Burkholderia association (12). Another chinch bug species, Cavelerius saccharivorus Okajima (Heteroptera: Lygaeoidea: Blissidae), also harbors Burkholderia spp.…”

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confidence: 99%

“…have been detected in the lumens of specialized crypts, at the fourth region of the midgut (M4) (Fig. 1), in the Southern chinch bug, Blissus insularis Barber (Hemiptera: Lygaeoidea: Blissidae) (12). This insect, a primary pest of St. Augustinegrass, Stenotaphrum secundatum (Walter) Kuntze (20,21), feeds on the grass phloem, resulting in diminished grass growth, yellowing and brown blade color, and the eventual death of grass patches (22,23).…”

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“…These symbionts usually colonize specialized regions of the midgut, are transmitted to offspring by egg smearing, symbiont-containing capsules, or coprophagy, and play a role in host insect fitness (3)(4)(5)(6)(7). Exocellular symbionts can provide nutrients to supplement the unbalanced diets of their host insects (1,(8)(9)(10))m thus conferring fitness advantages (e.g., body size, coloration, development, and growth) (11)(12)(13). In addition, these symbionts have been reported to elicit symbiont-mediated plant specialization (14), to modulate plant virus transmission (15,16), and/or to induce protection against pathogenic gut bacteria (17), protozoan parasites (18), and synthetic insecticides (19).…”

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Culturing and Characterization of Gut Symbiont Burkholderia spp. from the Southern Chinch Bug, Blissus insularis (Hemiptera: Blissidae)

Buss

Boucias

2016

Appl Environ Microbiol

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The phloem-feeding Southern chinch bug, Blissus insularis, harbors a high density of the exocellular bacterial symbiont Burkholderia in the lumen of specialized midgut crypts. Here we developed an organ culture method that initially involved incubating the B. insularis crypts in osmotically balanced insect cell culture medium. This approach enabled the crypt-inhabiting Burkholderia spp. to make a transition to an in vitro environment and to be subsequently cultured in standard bacteriological media. Examinations using ribotyping and BOX-PCR fingerprinting techniques demonstrated that most in vitro-produced bacterial cultures were identical to their crypt-inhabiting Burkholderia counterparts. Genomic and physiological analyses of gut-symbiotic Burkholderia spp. that were isolated individually from two separate B. insularis laboratory colonies revealed that the majority of individual insects harbored a single Burkholderia ribotype in their midgut crypts, resulting in a diverse Burkholderia community within each colony. The diversity was also exhibited by the phenotypic and genotypic characteristics of these Burkholderia cultures. Access to cultures of crypt-inhabiting bacteria provides an opportunity to investigate the interaction between symbiotic Burkholderia spp. and the B. insularis host. Furthermore, the culturing method provides an alternative strategy for establishing in vitro cultures of other fastidious insect-associated bacterial symbionts. M any plant-sap-feeding insects harbor exocellular bacterial symbionts in their digestive tracts (1, 2). These symbionts usually colonize specialized regions of the midgut, are transmitted to offspring by egg smearing, symbiont-containing capsules, or coprophagy, and play a role in host insect fitness (3-7). Exocellular symbionts can provide nutrients to supplement the unbalanced diets of their host insects (1, 8-10)m thus conferring fitness advantages (e.g., body size, coloration, development, and growth) (11-13). In addition, these symbionts have been reported to elicit symbiont-mediated plant specialization (14), to modulate plant virus transmission (15, 16), and/or to induce protection against pathogenic gut bacteria (17), protozoan parasites (18), and synthetic insecticides (19). IMPORTANCE An organ culture method was developed to establish in vitro cultures of a fastidiousRecently, Burkholderia spp. have been detected in the lumens of specialized crypts, at the fourth region of the midgut (M4) (Fig. 1), in the Southern chinch bug, Blissus insularis Barber (Hemiptera: Lygaeoidea: Blissidae) (12). This insect, a primary pest of St. Augustinegrass, Stenotaphrum secundatum (Walter) Kuntze (20,21), feeds on the grass phloem, resulting in diminished grass growth, yellowing and brown blade color, and the eventual death of grass patches (22, 23). Investigations of multiple B. insularis field populations demonstrated that complex Burkholderia ribotypes were present within and among the populations (12). The copy number of the Burkholderia 16S rRNA gene increased ...

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Accessing the Hidden Microbial Diversity of Aphids: an Illustration of How Culture-Dependent Methods Can Be Used to Decipher the Insect Microbiota

Grigorescu

Renoz

Sabri³

et al. 2017

Microb Ecol

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Microorganism communities that live inside insects can play critical roles in host development, nutrition, immunity, physiology, and behavior. Over the past decade, high-throughput sequencing reveals the extraordinary microbial diversity associated with various insect species and provides information independent of our ability to culture these microbes. However, their cultivation in the laboratory remains crucial for a deep understanding of their physiology and the roles they play in host insects. Aphids are insects that received specific attention because of their ability to form symbiotic associations with a wide range of endosymbionts that are considered as the core microbiome of these sap-feeding insects. But, if the functional diversity of obligate and facultative endosymbionts has been extensively studied in aphids, the diversity of gut symbionts and other associated microorganisms received limited consideration. Herein, we present a culture-dependent method that allowed us to successfully isolate microorganisms from several aphid species. The isolated microorganisms were assigned to 24 bacterial genera from the Actinobacteria, Firmicutes, and Proteobacteria phyla and three fungal genera from the Ascomycota and Basidiomycota phyla. In our study, we succeeded in isolating already described bacteria found associated to aphids (e.g., the facultative symbiont Serratia symbiotica), as well as microorganisms that have never been described in aphids before. By unraveling a microbial community that so far has been ignored, our study expands our current knowledge on the microbial diversity associated with aphids and illustrates how fast and simple culture-dependent approaches can be applied to insects in order to capture their diverse microbiota members.

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Detection and characterization of bacterial symbionts in the Heteropteran,Blissus insularis

Cited by 42 publications

References 46 publications

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Culturing and Characterization of Gut Symbiont Burkholderia spp. from the Southern Chinch Bug, Blissus insularis (Hemiptera: Blissidae)

Accessing the Hidden Microbial Diversity of Aphids: an Illustration of How Culture-Dependent Methods Can Be Used to Decipher the Insect Microbiota

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