Bacterial community of brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) revealed by high throughput amplicon sequencing

Authors

  • S Tyagi Department of Entomology & Agricultural Zoology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221 005, Uttar Pradesh, India https://orcid.org/0000-0003-0865-7130
  • N Srinivasa Department of Entomology & Agricultural Zoology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221 005, Uttar Pradesh, India https://orcid.org/0000-0002-3917-3713
  • R N Singh Department of Entomology & Agricultural Zoology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221 005, Uttar Pradesh, India https://orcid.org/0000-0002-3917-3713
  • V Arya Department of Entomology & Agricultural Zoology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221 005, Uttar Pradesh, India https://orcid.org/0000-0002-0901-5693

DOI:

https://doi.org/10.14719/pst.4184

Keywords:

insect microbiome, BPH symbionts, gut microflora, rice planthopper, 16S rDNA

Abstract

The bacterial symbionts of brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), a key sucking insect pest of rice in India and Asia, have been known to play many important physiological functions. Reports of yeast-like symbionts of N. lugens are widely known, but little is known about the bacterial microbes. In this study, the bacterial community structure and diversity were examined in N. Lugens collected from four major rice-growing regions of India utilizing culture-independent high throughput sequencing. The Mi seq technology identified a total of 1277 operational taxonomic units (OTUs) representing 4 phyla mainly (Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes) by analyzing 16S rDNA gene libraries. The major microbial groups were similar in the four samples, but their distribution patterns were different, especially in Raichur. While the top three bacterial genera linked to Imphal, Pantnagar, and Raichur were Methylobacterium, Sphingomonas, and Acinetobacter; Wolbachia accounted for 87.46% of the total genera found in Raipur. The identified dominant microbial groups have been known for their crucial role in insect’s life cycle. Diversity analysis tests revealed Raichur has the highest species diversity as determined by the high Shannon and Simpson index. According to ACE and Chao1 diversity estimates, Pantnagar has the highest species richness. Understanding the bacterial communities and studying their functional roles will help in formulating biological control strategies specific to this sucking pest.

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References

Liu XD, Sun QH. Early assessment of the yield loss in rice due to brown planthopper using a hyperspectral remote sensing method. Int J Pest Manag. 2016;62:205-13. https://doi.org/10.1080/09670874.2016.1174791

Jena M, Adak T, Rath PC, Gowda GB, Patil NB, Prasanthi G, Mohapatra SD. Paradigm shift of insect pests in rice ecosystem and their management strategy. Oryza. 2018;55(spl):82-89. https://doi.org/10.5958/2249-5266.2018.00010.3

Omkar, Tripathi AK. Sucking pests of cereals. In: Sucking Pests of Crops. Singapore: Springer; 2020. p. 3-53. https://doi.org/ 10.1007/978-981-15-6149-8_1

Rishi N. Significant plant virus diseases in India and a glimpse of modern disease management technology. J Gen Plant Pathol. 2009;75:1-18. https://doi.org/10.1007/s10327-008-0139-8

Akami MN, Njintang Y, Gbaye OA, Andongma AA, Rashid MA, Niu CY. Gut bacteria of the cowpea beetle mediate its resistance to dichlorvos and susceptibility to Lippia adoensis essential oil. Sci Rep. 2019;9:6435. https://doi.org/10.1038/s41598-019-42843-1

Fan HW, Noda H, Xie HQ, Suetsugu Y, Zhu QH, Zhang CX. Genomic analysis of an ascomycete fungus from the rice planthopper reveals how it adapts to an endosymbiotic lifestyle. Genome Bio Evol. 2015;7:2623-34. https://doi.org/10.1093/gbe/evv169

Tang T, Zhang Y, Cai T, Deng X, Liu C, Li J, et al. Antibiotics increased host insecticide susceptibility via collapsed bacterial symbionts reducing detoxification metabolism in the brown planthopper, Nilaparvata lugens. J Pest Sci. 2021;94:757-67. https://doi.org/10.1007/s10340-020-01294-8

Wang ZL, Pan HB, Wu W, Li MY, Yu XP. The gut bacterial flora associated with brown planthopper is affected by host rice varieties. Arch Microbiol. 2021;203:325-33. https://doi.org/10.1007/s00203-020-02013-8

Crotti E, Balloi A, Hamdi C, Sansonno L, Marzorati M, Gonella E. Microbial symbionts: a resource for the management of insect-related problems. Microbial Biotech. 2012;5:307-17. https://doi.org/10.1111/j.1751-7915.2011.00312.x

Mansour A, Mannaa M, Hewedy O, Ali MG, Jung H, Seo YS. Versatile roles of microbes and small RNAs in rice and planthopper interactions. Plant Pathol J. 2022;38:432-48. https://doi.org/10.5423/PPJ.RW.07.2022.0090

Arora AK, Douglas AE. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J Insect Physiol. 2017;103:10-17. https://doi.org/10.1016/j.jinsphys.2017.09.011

Berasategui A, Shukla S, Salem H, Kaltenpoth M. Potential applications of insect symbionts in biotechnology. Appl Microbiol Biotechnol. 2016;100:1567-77. https://doi.org/10.1007/s00253-015-7186-9

Chu D, Gao CS, Barro P, Zhang YJ, Wan FH, Khan IA. Further insights into the strange role of bacterial endosymbionts in whitefly, Bemisia tabaci: Comparison of secondary symbionts from biotypes B and Q in China. Bull Entomol Res. 2011;101:477. https://doi.org/10.1017.S0007485311000083

Mannaa M, Seo YS. Plants under the attack of allies: moving towards the plant pathobiome paradigm. Plants. 2021;10:125. https://doi.org/10.3390/plants10010125

Callahan BJ, Wong J, Heiner C, Oh S, Theriot CM, Gulati AS, et al. High-throughput amplicon sequencing of the full-length 16S rRNA gene with single-nucleotide resolution. Nucleic Acids Res. 2019;47:e103. https://doi.org/10.1093/nar/gkz569

Johnson JS, Spakowicz DJ, Hong BY, Hong BY, Petersen LM, Demkowicz P, et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Comm. 2019;10:5029. https://doi.org/10.1038/s41467-019-13036-1

Malathi VM, More RP, Anandham R, Gracy GR, Mohan M, Venkatesan T. Gut bacterial diversity of insecticide-susceptible and-resistant nymphs of the brown planthopper Nilaparvata lugens Stål (Hemiptera: Delphacidae) and elucidation of their putative functional roles. J Microbiol Biotech. 2018;28:976-86. https://doi.org/10.4014/jmb.1711.11039

Tyagi S, Narayana S, Singh RN, Srivastava CP, Twinkle S, Das SK, Jeer M. Migratory behaviour of Brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), in India as inferred from genetic diversity and reverse trajectory analysis. 3 Biotech. 2022;12:266. https://doi.org/10.1007/s13205-022-03337-6

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-97. https://doi.org/10.1093/nar/gkh340

Hou Y, Ma Z, Dong SZ, Chen YH, Yu XP. Analysis of yeast-like symbiote diversity in the brown planthopper (BPH), Nilaparvata lugens Stål, using a novel nested PCR-DGGE protocol. Curr Microbiol. 2013;67:263-70. https://doi.org/10.1007/s00284-013-0356-z

Zhang Y, Tang T, Li W, Cai T, Li J, Wan H. Functional profiling of the gut microbiomes in two different populations of the brown planthopper, Nilaparvata lugens. J Asia-Pacific Entomol. 2018;21:1309-14. https://doi.org/10.1016/j.aspen.2018.09.012

Liu W, Zhang X, Wu N, Ren Y, Wang X. High diversity and functional complementation of alimentary canal microbiota ensure small brown planthopper to adapt different biogeographic environments. Front Microbiol. 2020;10:2953. https://doi.org/10.3389/fmicb.2019.02953

Saranya M, Kennedy JS, Anandham R, Manikandan A. Characterization and functional significance of bacteria associated with rugose spiralling whitefly, Aleurodicus rugioperculatus Martin (Hemiptera: Aleyrodidae) reared on guava plants. Appl Entomol Zool. 2022;57:323-31. https://doi.org/10.1007/s13355-022-00791-9

Wang ZL, Wang TZ, Zhu HF, Pan HB, Yu XP. Diversity and dynamics of microbial communities in brown planthopper at different developmental stages revealed by high?throughput amplicon sequencing. Insect Sci. 2020;27:883-94. https://doi.org/10.1111/1744-7917.12729

Tang M, Lu L, Jing SL, Zhu LL, He GC. Bacterial symbionts of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Appl Environ Microbiol. 2010;76:1740-45. https://doi.org/10.1128/AEM.02240-09

Zhang JH, Yu N, Xu XX, Liu ZW. Community structure, dispersal ability and functional profiling of microbiome existing in fat body and ovary of the brown planthopper, Nilaparvata lugens. Insect Sci. 2019;26:683-94. https://doi.org/10.1111/1744-7917.12575

Klammsteiner T, Walter A, Bogataj T, Heussler CD. The core gut microbiome of black soldier fly (Hermetia illucens) larvae raised on low-bioburden diets. Front Microbiol. 2020;11:993. https://doi.org/10.3389/fmicb.2020.00993

Tegtmeier D, Hurka S, Klüber P, Brinkrolf K, Heise P, Vilcinskas A. Cottonseed press cake as a potential diet for industrially farmed black soldier fly larvae triggers adaptations of their bacterial and fungal gut microbiota. Front Microbiol. 2021;12:634503. https://doi.org/10.3389/fmicb.2021.634503

Yun JH, Roh SW, Whon TW, Jung MJ, Kim MS, Park DS, et al. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage and phylogeny of host. Appl Environ Microbiol. 2014;80:5254-64. https://doi.org/10.1128/AEM.01226-14

Ohkuma M, Noda S, Hongoh Y, Kudo T. Diverse bacteria related to the bacteroides subgroup of the CFB phylum within the gut symbiotic communities of various termites. J Agric Chem Soc Jap. 2002;6:78-84. https://doi.org/10.1271/bbb.66.78

Schloss PD, Delalibera I, Handelsman J, Raffa KF. Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environ Entomol. 2006;35:625-29. https://doi.org/10.1603/0046-225X-35.3.625

Bing XL, Zhao DS, Peng CW, Huang HJ, Hong XY. Similarities and spatial variations of bacterial and fungal communities in field rice planthopper (Hemiptera: Delphacidae) populations. Insect Sci. 2020;27:947-63. https://doi.org/10.1111/1744-7917.12782

Qu LY, Lou YH, Fan HW, Ye YX, Huang HJ, Hu MQ, et al. Two endosymbiotic bacteria, Wolbachia and Arsenophonus, in the brown planthopper Nilaparvata lugens. Symbiosis. 2013;61:47-53. https://doi.org/10.1007/s13199-013-0256-9

Robinson CJ, Bohannan BJM, Young VB. From structure to function: the ecology of host-associated microbial communities. Microbiol Molecular Biol Rev. 2010;74:453. https://doi.org/10.1128/mmbr.00014-10

Ren Z, Zhang Y, Cai T, Mao K, Xu Y, Li C, et al. Dynamics of microbial communities across the life stages of Nilaparvata lugens (Stål). Microbial Ecol. 2022;83:1049-58. https://doi.org/10.1007/s00248-021-01820-w

Hosokawa T, Ishii Y, Nikoh N, Fujie M, Satoh N, Fukatsu T. Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations. Nat Microbiol. 2016;1:1-7. https://doi.org/10.1038/nmicrobiol.2015.11

Brown MR. Environment dominates host factors in shaping mosquito gut microbiota. Scand J Psychol. 2015;56:458-66.

Kelly PH, Bahr SM, Serafim TD, Ajami NJ, Petrosino JF, Meneses C, et al. The gut microbiome of the vector Lutzomyia longipalpis is essential for survival of Leishmania infantum. mBio. 2017;8:e1121-16. https://doi.org/10.1128/mbio.01121-16

Xiao Q, Wang L, Chen SQ, Zheng CY, Lu YY, Xu YJ. Gut microbiome composition of the fire ant Solenopsis invicta: an integrated analysis of host genotype and geographical distribution. Microbiol Spectrum. 2023;11:e03585-22. https://doi.org/10.1128/spectrum.03585-22

Published

28-12-2024 — Updated on 01-01-2025

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1.
Tyagi S, Srinivasa N, Singh RN, Arya V. Bacterial community of brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) revealed by high throughput amplicon sequencing. Plant Sci. Today [Internet]. 2025 Jan. 1 [cited 2025 Jan. 6];12(1). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/4184

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