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Gut Microbiota of Tenebrio Molitor and Their Response to Environmental Change Jaejoon Jung1,2, Aram Heo1, Yong Woo Park1, Ye Ji Kim1, Hyelim Koh1, and Woojun Park1*

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Gut Microbiota of Tenebrio Molitor and Their Response to Environmental Change Jaejoon Jung1,2, Aram Heo1, Yong Woo Park1, Ye Ji Kim1, Hyelim Koh1, and Woojun Park1* J. Microbiol. Biotechnol. (2014), 24(7), 888–897 http://dx.doi.org/10.4014/jmb.1405.05016 Research Article Review jmb Gut Microbiota of Tenebrio molitor and Their Response to Environmental Change Jaejoon Jung1,2, Aram Heo1, Yong Woo Park1, Ye Ji Kim1, Hyelim Koh1, and Woojun Park1* 1Laboratory of Molecular Environmental Microbiology, Department of Environmental Science and Ecological Engineering, Korea University, Seoul 136-713, Republic of Korea 2Institute of Life Science and Natural Resources, Korea University, Seoul 136-713, Republic of Korea Received: May 8, 2014 Revised: May 23, 2014 A bacterial community analysis of the gut of Tenebrio molitor larvae was performed using Accepted: May 26, 2014 pyrosequencing of the 16S rRNA gene. A predominance of genus Spiroplasma species in phylum Tenericutes was observed in the gut samples, but there was variation found in the community composition between T. molitor individuals. The gut bacteria community structure First published online was not significantly affected by the presence of antibiotics or by the exposure of T. molitor May 27, 2014 larvae to a highly diverse soil bacteria community. A negative relationship was identified *Corresponding author between bacterial diversity and ampicillin concentration; however, no negative relationship Phone: +82-2-3290-3067; was identified with the addition of kanamycin. Ampicillin treatment resulted in a reduction in Fax: +82-2-953-0737; the bacterial community size, estimated using the 16S rRNA gene copy number. A detailed E-mail: [email protected] phylogenetic analysis indicated that the Spiroplasma-associated sequences originating from the T. molitor larvae were distinct from previously identified Spiroplasma type species, implying the presence of novel Spiroplasma species. Some Spiroplasma species are known to be insect pathogens; however, the T. molitor larvae did not experience any harmful effects arising from the presence of Spiroplasma species, indicating that Spiroplasma in the gut of T. molitor larvae do not act as a pathogen to the host. A comparison with the bacterial communities found in other insects (Apis and Solenopsis) showed that the Spiroplasma species found in this study were pISSN 1017-7825, eISSN 1738-8872 specific to T. molitor. Copyright© 2014 by The Korean Society for Microbiology Keywords: Tenebrio molitor, Spiroplasma, Tenericutes, ampicillin, pyrosequencing and Biotechnology Introduction microbiota of insects usually represents a very simple community. This is because the environment of the gut is The insect gut is a distinctive habitat for microbial quite selective for a specific bacterial group; in addition, colonization. Bacterial communities are thought to perform some insects have a regulatory system for maintaining many roles that are beneficial to their hosts. Insects are specific gut communities [21, 22]. often dependent on gut bacteria to perform basic biological Spiroplasma (class Mollicutes) is a genus that is often functions such as aiding in the digestion of low-nutrient found in the gut microbiota of insects. Spiroplasma species food, protection from disease or predators, mating, and are non-cell-wall bacteria with a spiral cell morphology. reproduction [2, 4, 23]. To understand the relationship There are four clades of Spiroplasma based on the 16S rRNA between gut microbiota and many aspects of insect life, genes; namely, the Apis, Mycoides, Citri, and Ixodetis clades. community analysis has been performed across a diverse The isolation sources of these Spiroplasma species are range of insects, including the bumble bee (genus Bombus), roughly congruent with phylogenetic trees [8]. Spiroplasma honey bee (genus Apis), leafcutter bee (genus Megachile), is a major endosymbiont of Drosophila [24]. Endocellular ants (genera Cephalotes and Solenopsis), Drosophila, and and extracellular associations with a variety of plants and many genera of termites [3, 5, 10, 13, 14, 26]. The gut arthropods have also been reported. Several Spiroplasma July 2014 ⎪ Vol. 24⎪ No. 7 889 Jung et al. species have been reported to possess male-killing pathogenic larvae for 5 or 10 days, and the guts were dissected from 10 activity of many insects, including Drosophila, ladybird individuals. For brevity in this manuscript, we have named the beetles, and butterflies [15]. However, not all Spiroplasma samples with an abbreviation of the name of the antibiotics and species are pathogens, and infection with Spiroplasma does with the concentration. For example, Amp 100 means the sample not always have detrimental effects. was exposed to 100 µg/ml ampicillin. Although there are various modifications that can occur, in general, the insect gut is known to Tenebrio molitor is a species of darkling beetle (order have a three-part structure: foregut, midgut, and hindgut [11]. The Coleoptera), which produces larvae that are commonly structure of the gut of T. molitor larvae was not visibly separated. called mealworms. Acting as decomposers in the natural Consequently, DNA extraction and analysis were performed environment, they feed on decaying plant materials and without considering the gut structure. dead insects. In addition, as a result of its easy handling and non-fastidious culture conditions, T. molitor is used as Denaturing Gradient Gel Electrophoresis (DGGE) a pet food, an educational material, and as a biological To investigate the variation in the bacterial communities of research model [27]. Whereas the relationship between T. molitor larvae, DGGE was performed on samples from nine microorganisms and several insects, such as termites and T. molitor larvae. The gut was dissected from T. molitor larvae and honey bees, has been well-studied by many researchers, DNA was isolated using the NucleoSpin system (Machery-Nagel; the role of the microorganisms residing in T. molitor is Germany) according to the manufacturer’s instructions. The rarely understood. To enhance the understanding of the bacterial 16S rRNA gene was amplified using the 27F and 1492R interactions between microbiota and T. molitor, we conducted primers. The quantity of template DNA used in the protocol was 10 ng. The polymerase chain reaction (PCR) protocol utilized a bacterial community analysis from the gut of T. molitor included 5 min at 94°C, followed by 20 cycles of 45 sec at 94°C, larvae. We evaluated the effect of antibiotics (ampicillin 45 sec at 55°C, and 45 sec at 72°C. A final extension step was and kanamycin) on the gut bacterial community. To our performed for 5 min at 72°C. The PCR products from this reaction best knowledge, studies on the exposure of gut microbiota were used as template DNA for the second PCR step using the of T. molitor to antibiotics has not been reported. To further b341GC and 758r primers. The same PCR protocol was used for evaluate the response of the gut microbial community to its the second PCR step with the exception of 35 cycles in place of 20. environment, we provided the bacterial community with DGGE was performed using the D-Code system (Bio-Rad; USA) great diversity in its environment by culturing the larvae in for 16 h at 60°C and 70 V. The denaturants (urea and formamide) a mixture of soil and bran. Finally, we compared the range was from 40% to 60%. microbial community structure of the gut of T. molitor larvae with those from other insects to provide insight into Bacterial Community Analysis Using Pyrosequencing the insect gut microbiota. This is the first report of a In order to perform a culture-independent bacterial community bacterial community analysis in the gut of T. molitor. analysis, pyrosequencing of the bacterial 16S rRNA gene sequence was performed. Hypervariable regions (V1–V3) were amplified using the 27F and 518R primers containing 10 bp barcode sequences. Materials and Methods The construction of a sequencing library and pyrosequencing Culture of T. molitor Larvae and Injection of Antibiotics using the GS-FLX Titanium system were performed by Macrogen T. molitor larvae were purchased from a local market. The body Inc. (Republic of Korea). Short (<180 bp) and low-quality reads weight of the larvae used in the study ranged from 50 to 60 mg. were eliminated from the raw sequencing data using Mothur Antibiotics were either injected directly into the gut or were software [30]. The demultiplexed sequencing data were normalized added to the diet of the larvae. The concentrations of injected by subsampling 8,733 reads from all samples using Mothur. This antibiotics were 50 and 100 µg/ml for ampicillin, and 1, 5, 10, and number was selected because it was the smallest number of reads 50 µg/ml for kanamycin. In order to add antibiotics to bran, from the samples. Taxonomic classification and the calculation of antibiotics dissolved in distilled water were thoroughly mixed diversity indices were performed using the Ribosomal Database with bran and the distilled water was removed by evaporation. Project (RDP) database (http://pyro.cme.msu.edu/) [9]. Sequence The final concentrations of the antibiotics in the bran were 300, alignment, clustering of the sequences using a variety of cutoff 500, 700, and 900 µg/ml for ampicillin (Amp), and 100, 200, 300, values, and the calculation of diversity indices were performed and 500 µg/ml for kanamycin (Km). When the larvae were using the RDP database. QIIME was used to compare the bacterial cultured in soil, the soil and bran were mixed at a 1:1 (v/v) ratio. communities and create an OTU network visualized using Cytoscape Following their exposure to antibiotics by injection, we incubated software [31]. Raw pyrosequencing data from previously published the larvae for 5 days and the guts were dissected from 10 literature were downloaded from the NCBI SRA database and individuals. In the antibiotic soil conditions, we incubated the were processed with an SRA toolkit and Mothur software. J. Microbiol. Biotechnol. Gut Microbiota of Tenebrio molitor 890 Quantitative Real-Time PCR (qPCR) for Estimating the 16S was expected, because many sequences were not taxonomically rRNA Gene Copy Numbers affiliated at the gene level.
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