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Bacterial Communities in Bacteriomes, Ovaries and Testes of three Geographical Populations of a Sap-Feeding Insect, Platypleura kaempferi (Hemiptera: Cicadidae)

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Abstract

Mutualistic associations between symbiotic bacteria and their insect hosts are widespread. The bacterial diversity and community composition within hosts may play an important role in shaping insect biology, ecology, and evolution. Here, we focused on the bacterial communities in bacteriomes, ovaries and testes of three representative populations of the cicada Platypleura kaempferi (Fabricius) using high-throughput 16S rRNA amplicon sequencing approach combined with light microscopy and confocal imaging approach. The obligate symbiont Sulcia was detected in all the examined samples, which showed a relatively high abundance in most bacteriomes and ovaries. The unclassified OTUs formerly identified as an unclassified Rhizobiales bacterium was demonstrated to be the co-obligate symbiont Hodgkinia, which showed 100% infection rate in all the examined samples and had an especially high abundance in most bacteriomes and ovaries. Hodgkinia and Sulcia occupy the central and peripheral bacteriocytes of each bacteriome unit, respectively. Cluster analysis revealed that the bacterial communities in bacteriomes, ovaries and testes of Zhouzhi and Ningshan populations separated strongly from each other. Significant difference was also detected between the Yangling and Ningshan populations, but no significant difference was detected between the Yangling and Zhouzhi populations. This may be related to the difference of host plants and genetic differentiation of these populations. Our findings show that the bacterial communities can be influenced by the population differentiation of the host cicadas and/or the host plants of cicadas, which improve our understanding of the associations between the bacterial community and population differentiation of sap-feeding insects.

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Data Availability

All sequences have been submitted to GenBank (Accession Nos.: MT672251–MT672255, MT762257–MT672264, MW590200 and MW629023–MW629053). The raw reads of 16S rRNA amplicon sequencing were deposited in the NCBI Sequence Read Archive (SRA) database under BioProject accession number PRJNA640760.

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Acknowledgements

We thank Zhi Huang and Lingyan Bai (Northwest A&F University, China) for specimen collection.

Funding

This study was supported by the National Natural Science Foundation of China (Grant Numbers: 31772505, 32070476).

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Authors and Affiliations

  1. Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Dandan Wang, Yunxiang Liu, Yan Su & Cong Wei

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  2. Yunxiang Liu
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  3. Yan Su
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Contributions

DW, YL and CW compiled and designed the experiment. All the authors contributed to the interpretation of results and made a significant contribution to the preparation of the manuscript. All the authors have read, revised, and approved the final version of the manuscript.

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Correspondence to Cong Wei.

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The authors declare that they have no conflict of interest.

Ethical Approval

This study was carried out in full compliance with the laws of the People’s Republic of China. No specific permits were required for our field investigation. All studied species are not included in the ‘List of Protected Animals in China’.

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284_2021_2435_MOESM1_ESM.xlsx

Table S1 Sample information of P. kaempferi used for amplicon sequencing. Table S2 Intraspecific genetic distance of P. kaempferi and interspecific genetic distance of Platypleura species based on COI gene. Table S3 Number of 16S rDNA sequences after quality filtering, de-noising, and chimera removal, number of operational taxonomic units, and alpha diversity metrics of bacteriomes and reproductive organs of P. kaempferi. Table S4 Relative abundance of the top ten bacteria in each sample of P. kaempferi. Table S5 The relative abundance of the 25 OTUs that showed a high similarity (> 98%) to partial sequence of Hodgkinia based on amplicon sequencing (XLSX 34 KB)

284_2021_2435_MOESM2_ESM.tif

Fig. S1 Sampling locations of P. kaempferi. (a) Satellite image. (b) Land cover of the three sampling locations constructed using the Engaging Citizens in Environmental Monitoring (https://geo-wiki.org/Security/login?BackURL=%2FApplication%2Findex.php) (TIF 11255 KB)

284_2021_2435_MOESM3_ESM.tif

Fig. S2 (a) Rarefaction curve of the 33 samples. Horizontal axis: the amount of effective sequencing data; vertical axis: the observed number of operational taxonomic units. (b) Rank abundance curve of the 33 samples. Horizontal axis: the ordinal sorted by OTUs abundance; vertical axis: the relative abundance of the corresponding OTUs (TIF 1269 KB)

284_2021_2435_MOESM4_ESM.tif

Fig. S3 Violin plots showing alpha diversity index of three different geographical populations of P. kaempferi. (a) Differences of ACE index. (b) Differences of Shannon index. The P value is represented by “*”. * 0.01 < P < 0.05, ** 0.001 < P < 0.01, *** P < 0.001. Note: the number of repetitions in ovaries and testes of Yangling population are less than three, so these two groups were not included in these plots. Zt, Zo, Zmb, and Zfb, respectively, represent the testes, ovaries, male’s bacteriomes, and female’s bacteriomes of P. kaempferi occurring in Zhouzhi; Yt, Yo, Ymb, and Yfb, respectively, represent the testes, ovaries, male’s bacteriomes, and female’s bacteriomes of P. kaempferi occurring in Yangling; Nt, No, Nmb, and Nfb, respectively, represent the testes, ovaries, male’s bacteriomes, and female’s bacteriomes of P. kaempferi occurring in Ningshan (TIF 514 KB)

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Wang, D., Liu, Y., Su, Y. et al. Bacterial Communities in Bacteriomes, Ovaries and Testes of three Geographical Populations of a Sap-Feeding Insect, Platypleura kaempferi (Hemiptera: Cicadidae). Curr Microbiol 78, 1778–1791 (2021). https://doi.org/10.1007/s00284-021-02435-7

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