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Impacts of Antibiotic and Bacteriophage Treatments on the Gut-Symbiont-Associated Blissus insularis (Hemiptera: Blissidae).

ABSTRACT: The Southern chinch bug, Blissus insularis, possesses specialized midgut crypts that harbor dense populations of the exocellular symbiont Burkholderia. Oral administration of antibiotics suppressed the gut symbionts in B. insularis and negatively impacted insect host fitness, as reflected by retarded development, smaller body size, and higher susceptibility to an insecticide, bifenthrin. Considering that the antibiotics probably had non-lethal but toxic effects on host fitness, attempts were conducted to reduce gut symbionts using bacteriophage treatment. Soil-lytic phages active against the cultures of specific Burkholderia ribotypes were successfully isolated using a soil enrichment protocol. Characterization of the BiBurk16MC_R phage determined its specificity to the Bi16MC_R_vitro ribotype and placed it within the family Podoviridae. Oral administration of phages to fifth-instar B. insularis, inoculated with Bi16MC_R_vitro as neonates had no deleterious effects on host fitness. However, the ingested phages failed to impact the crypt-associated Burkholderia. The observed inactivity of the phage was likely due to the blockage of the connection between the anterior and posterior midgut regions. These findings suggest that the initial colonization by Burkholderia programs the ontogeny of the midgut, providing a sheltered residence protected from microbial antagonists.

SUBMITTER: Xu Y

PROVIDER: S-EPMC5198209 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Impacts of Antibiotic and Bacteriophage Treatments on the Gut-Symbiont-Associated Blissus insularis (Hemiptera: Blissidae).

Xu Yao Y Buss Eileen A EA Boucias Drion G DG

Insects 20161103 4

The Southern chinch bug, Blissus insularis, possesses specialized midgut crypts that harbor dense populations of the exocellular symbiont Burkholderia. Oral administration of antibiotics suppressed the gut symbionts in B. insularis and negatively impacted insect host fitness, as reflected by retarded development, smaller body size, and higher susceptibility to an insecticide, bifenthrin. Considering that the antibiotics probably had non-lethal but toxic effects on host fitne ...[more]

PMID: 27827869

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Project description:UnlabelledThe 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.ImportanceAn organ culture method was developed to establish in vitro cultures of a fastidious Burkholderia symbiont associated with the midgut crypts of the Southern chinch bug, Blissus insularis The identities of the resulting cultures were confirmed using the genomic and physiological features of Burkholderia cultures isolated from B. insularis crypts, showing that host insects maintained the diversity of Burkholderia spp. over multiple generations. The availability of characterized gut-symbiotic Burkholderia cultures provides a resource for genetic manipulation of these bacteria and for examination of the mechanisms underlying insect-bacterium symbiosis.

Project description:BackgroundFecal microbiota transplantation (FMT) and fecal virome transplantation (FVT, sterile filtrated donor feces) have been effective in treating recurrent Clostridioides difficile infections, possibly through bacteriophage-mediated modulation of the gut microbiome. However, challenges like donor variability, costly screening, coupled with concerns over pathogen transfer (incl. eukaryotic viruses) with FMT or FVT hinder their wider clinical application in treating less acute diseases.MethodsTo overcome these challenges, we developed methods to broaden FVT's clinical application while maintaining efficacy and increasing safety. Specifically, we employed the following approaches: (1) chemostat-fermentation to reproduce the bacteriophage FVT donor component and remove eukaryotic viruses (FVT-ChP), (2) solvent-detergent treatment to inactivate enveloped viruses (FVT-SDT), and (3) pyronin-Y treatment to inhibit RNA virus replication (FVT-PyT). We assessed the efficacy of these processed FVTs in a C. difficile infection mouse model and compared them with untreated FVT (FVT-UnT), FMT, and saline.ResultsFVT-SDT, FVT-UnT, and FVT-ChP reduced the incidence of mice reaching the humane endpoint (0/8, 2/7, and 3/8, respectively) compared to FMT, FVT-PyT, and saline (5/8, 7/8, and 5/7, respectively) and significantly reduced the load of colonizing C. difficile cells and associated toxin A/B levels. There was a potential elimination of C. difficile colonization, with seven out of eight mice treated with FVT-SDT testing negative with qPCR. In contrast, all other treatments exhibited the continued presence of C. difficile. Moreover, the results were supported by changes in the gut microbiome profiles, cecal cytokine levels, and histopathological findings. Assessment of viral engraftment following FMT/FVT treatment and host-phage correlations analysis suggested that transfer of phages likely were an important contributing factor associated with treatment efficacy.ConclusionsThis proof-of-concept study shows that specific modifications of FVT hold promise in addressing challenges related to donor variability and infection risks. Two strategies lead to treatments significantly limiting C. difficile colonization in mice, with solvent/detergent treatment and chemostat propagation of donor phages emerging as promising approaches. Video Abstract.

Dataset Information

Impacts of Antibiotic and Bacteriophage Treatments on the Gut-Symbiont-Associated Blissus insularis (Hemiptera: Blissidae).

Publications

Impacts of Antibiotic and Bacteriophage Treatments on the Gut-Symbiont-Associated Blissus insularis (Hemiptera: Blissidae).

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