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Environmental Factors and the Symbiont Cardinium Influence the Bacterial Microbiome of Spider Mites Across the Landscape

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Abstract

Microbes play a key role in the biology, ecology, and evolution of arthropods. Despite accumulating data on microbial communities in arthropods that feed on plants using piercing-sucking mouthparts, we still lack a comprehensive understanding of the composition and assembly factors of the microbiota, particularly in field-collected spider mites. Here, we applied 16S rRNA amplicon sequencing to investigate the characters of the bacterial community in 140 samples representing 420 mite individuals, belonging to eight Tetranychus species (Acari: Tetranychidae) collected from 26 sites in China. The results showed that the bacterial composition of spider mites varied significantly among different species, locations, and plants. The environment showed a significant influence on the bacterial community of spider mites, with different relative contributions. Latitude and precipitation were found to be the main factors influencing the bacterial community composition. The dissimilarity of bacterial community and geographical distance between mite locations were significantly correlated. The assembly of spider mite bacterial communities seemed to be mainly influenced by stochastic processes. Furthermore, the symbiont Cardinium was found to be important in shaping the microbiota of many Tetranychus species. The relative abundance of Cardinium was > 50% in T. viennensis, T. urticae G, T. urticae R, and T. turkestani. Removing Cardinium reads from our analysis significantly changed Shannon diversity index and weighted beta diversity in these species. Altogether, this study provides novel insights into bacterial diversity patterns that contribute to our knowledge of the symbiotic relationships between arthropods and their bacterial communities.

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Data Availability

The sequencing data have been deposited in the NCBI Sequence Read Archive (SRA) database with the BioProject number PRJNA555522. All supplementary files and associated dataset are available from Zenodo under the https://doi.org/10.5281/zenodo.8150083.

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Acknowledgements

We thank Prof. Jing-Tao Sun from Nanjing Agricultural University and Ary Hoffmann from University of Melbourne for the help on improving the manuscript. We thank the high-performance computing platform of Bioinformatics Center, Nanjing Agricultural University, for support with bioinformatical analysis.

Funding

This study was supported by the National Key R&D Program of China (No. 2022YFC2601000), National Natural Science Foundation of China (No. 32001905 and 32020103011), Natural Science Foundation of Jiangsu Province (No. BK20211213), and the Fundamental Research Funds for the Central Universities (No. KJQN202110). The funders played no role in study design, data collection, analysis and interpretation of data, or the writing of this manuscript.

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  1. Department of Entomology, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, China

    Huan-Huan Liu, Lei Chen, Hui-Biao Shao, Shuo Gao, Xiao-Yue Hong & Xiao-Li Bing

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Huan-Huan Liu, Lei Chen, Hui-Biao Shao, Shuo Gao, Xiao-Yue Hong, and Xiao-Li Bing. The first draft of the manuscript was written by Huan-Huan Liu and Xiao-Li Bing. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Supplementary Information

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Supplementary file1 (DOCX 2940 KB)

248_2023_2314_MOESM2_ESM.csv

Supplementary file2 (CSV 36 KB) Sample information of spider mites and environmental factor information of collection sites

Supplementary file3 (XLSX 5391 KB) Relative abundance of bacteria at genus level in spider mites

Supplementary file4 (CSV 12 KB) Statistical details of alpha and beta diversity analysis

248_2023_2314_MOESM5_ESM.xlsx

Supplementary file5 (XLSX 12 KB) Mantel Test of the effect of Environmental factors on the bacterial Community of spider mites

Supplementary file6 (CSV 12 KB) Statistical details of alpha and beta diversity analysis after removing Cardinium

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Liu, HH., Chen, L., Shao, HB. et al. Environmental Factors and the Symbiont Cardinium Influence the Bacterial Microbiome of Spider Mites Across the Landscape. Microb Ecol 87, 1 (2024). https://doi.org/10.1007/s00248-023-02314-7

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