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. 2014 Sep;80(17):5254-64.
doi: 10.1128/AEM.01226-14. Epub 2014 Jun 13.

Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host

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Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host

Ji-Hyun Yun et al. Appl Environ Microbiol. 2014 Sep.

Abstract

Insects are the most abundant animals on Earth, and the microbiota within their guts play important roles by engaging in beneficial and pathological interactions with these hosts. In this study, we comprehensively characterized insect-associated gut bacteria of 305 individuals belonging to 218 species in 21 taxonomic orders, using 454 pyrosequencing of 16S rRNA genes. In total, 174,374 sequence reads were obtained, identifying 9,301 bacterial operational taxonomic units (OTUs) at the 3% distance level from all samples, with an average of 84.3 (± 97.7) OTUs per sample. The insect gut microbiota were dominated by Proteobacteria (62.1% of the total reads, including 14.1% Wolbachia sequences) and Firmicutes (20.7%). Significant differences were found in the relative abundances of anaerobes in insects and were classified according to the criteria of host environmental habitat, diet, developmental stage, and phylogeny. Gut bacterial diversity was significantly higher in omnivorous insects than in stenophagous (carnivorous and herbivorous) insects. This insect-order-spanning investigation of the gut microbiota provides insights into the relationships between insects and their gut bacterial communities.

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Figures

FIG 1
FIG 1
Abundance and composition of gut microbiota in 218 insect species. 18S rRNA gene sequences were aligned using the ClustalW program, and a phylogenetic tree was constructed based on the neighbor-joining algorithm, using the MEGA5 program. (Left) The 21 insect orders in the phylogenetic tree are represented by colored lines. (Right) The compositions of the gut microbiota at the phylum level, based on 16S rRNA gene sequences, are shown in the bar graph. The insect species in the phylogenetic tree are described in Table S1 in the supplemental material.
FIG 2
FIG 2
Similarities of bacterial 16S rRNA gene sequences in different orders of insects. % ID indicates % identity.
FIG 3
FIG 3
Distribution of 4 bacterial symbionts in the insect gut. The relative abundances of the symbionts in 21 insect orders (a) and their infection frequencies (b) are shown.
FIG 4
FIG 4
Relative abundances of insect gut bacterial groups, categorized by their oxygen requirements, according to the hosts' environmental habitat, diet, developmental stage, and phylogenetic position. White, gray, and black bars represent aerobes, facultative anaerobes, and anaerobes, respectively. The bacteria were characterized based on previous descriptions of the phenotypic features of each of the bacterial genera, as shown in Table S3 in the supplemental material. Asterisks indicate statistically significant differences among all pairs of relative abundances (*, P < 0.05; **, P < 0.01).
FIG 5
FIG 5
Bacterial diversity in insect gut microbiota with respect to the hosts' environmental habitat, diet, developmental stage, and phylogeny. The amount of bacterial diversity was determined by comparing the numbers of OTUs (top) and the Shannon diversity indices (bottom). Asterisks indicate statistically significant differences among all pairs of values (*, P < 0.05; **, P < 0.01; ***, P < 0.001).
FIG 6
FIG 6
Diversity of gut microbiota of Apis mellifera, Illeis koebelei, and Lycorma delicatula. The gut microbiota of honeybees (Apis mellifera) were collected from separate locations (CG [site 12 in Fig. S1 in the supplemental material], Chilgok-Gun; JG [site 13], Jinan-Gun; WS [site 5], Wonju-Si; SS [site 6], Seosan-Si; and GG [site 10], Goesan-Gun) or reported in previous studies. (a) Compositions of gut microbiota at the phylum level. (b) PCA showing the gut microbiota of A. mellifera collected from separate locations or reported in previous studies. Bacterial community analysis and PCA were performed using data generated in this study and from previous studies. The bacterial distributions of gut microbiota in I. koebelei (planthopper) (c) and L. delicatula (yellow ladybird) (d) collected at different insect developmental stages are shown. (e) Numbers of shared OTUs of the bacterial community at the different developmental stages of I. koebelei and L. delicatula. Shared OTUs in L. delicatula nymphs were not observed. The insect samples of I. koebelei were collected from the same region, except for the "Adult 4" sample. (f) PCoA showing the gut microbiota of I. koebelei and L. delicatula collected at different insect developmental stages.
FIG 7
FIG 7
Composition of the insect gut microbiota compared with that of the mammalian gut microbiota from the study of Ley et al. (38). Principle coordinate analysis was performed using a PHYLIP-formatted distance matrix based on Jaccard values.

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