Abstract
The Indian lac insect, Kerria lacca (Kerr) is an industrially important insect because of its resin and pigment synthesizing capacity. Lac insects are phytophagous, sedentary almost throughout life and depend on phloem sap which is nutritionally imbalanced diet. Hence, it is postulated that endosymbionts are obligatory for their survival. Understanding the dynamics of microbiome of the lac insect is essential to unravel the complex interplay between microbes and lac insects. To study the diversity of endosymbiotic bacteria of lac insects, V3-V4 metagenome sequencing of neonate nymphs (crawlers) and the commercially important life stage, adult female lac insects were carried out using Illumina Hiseq 2500 platform. A total of 1646 OTUs (Operational Taxonomic Units) were obtained from both samples. The microbial diversity of crawlers and adult female lac insects was found to be different which could be due to the differences in morphology and physiology of those stages. More bacterial diversity and richness were found in crawlers compared to the adult female insects. Proteobacteria was the most abundant phylum in both stages, followed by Bacteroidetes and Actinobacteria. Wolbachia and Pantoea were the predominant bacterial genera in the female lac insects. This paper is the first record on the study of bacterial composition of lac insect life stages using NGS technique. Evaluating the role of these microbes in lac insects may help in improving lac yield and productivity.
Similar content being viewed by others
Data availability
Data have been submitted to the NCBI Sequence Read Archive (SRA) under accession number PRJNA638760.
References
Ali H, Muhammad A, Sanda NB, Huang Y, Hou Y (2019) Pyrosequencing uncovers a shift in bacterial communities across life stages of Octodonta nipae (Coleoptera: Chrysomelidae). Front Microbiol. https://doi.org/10.3389/fmicb.2019.00466
Bozorov TA, Rasulov BA, Zhang D (2019) Characterization of the gut microbiota of invasive Agrilus mali Matsumara (Coleoptera: Buprestidae) using high-throughput sequencing: uncovering plant cell-wall degrading bacteria. Sci Rep. https://doi.org/10.1038/s41598-019-41368-x
Calcagnile M, Tredici SM, Talà A, Alifano P (2019) Bacterial semiochemicals and trans kingdom interactions with insects and plants. Insects 10:441. https://doi.org/10.3390/insects10120441
Cao Y, Fanning S, Proos S, Jordan K, Srikumar S (2017) A Review on the applications of Next Generation Sequencing technologies as applied to food-related microbiome studies. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01829
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, PeÃsa AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Charlat S, Hurst GDD, Merçot H (2003) Evolutionary consequences of Wolbachia infections. Trends Genet 19:217–223
Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. PNAS 106(52):22427–22432
García MM, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB (2016) ScaleNet: A literature-based model of scale insect biology and systematics. Database. https://doi.org/10.1093/database/bav118
Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. https://doi.org/10.1126/science.1162418
Itoh H, Tago K, Hayatsu M, Kikuchi Y (2018) Detoxifying symbiosis: microbe-mediated detoxification of phytotoxins and pesticides in insects. Nat Prod Rep 35:434–454. https://doi.org/10.1039/c7np00051k
Jones RT, Sanchez LG, Fierer N (2013) A cross-taxon analysis of insect-associated bacterial diversity. PloS One 8(4):e61218. https://doi.org/10.1371/journal.pone.0061218
Kaczmarczyk A, Kucharczyk H, Kucharczyk M, Kapusta P, Sell J, Zielińska S (2018) First insight into microbiome profile of fungivorous thrips Hoplothrips carpathicus (Insecta: Thysanoptera) at different developmental stages: molecular evidence of Wolbachia endosymbiosis. Sci Rep. https://doi.org/10.1038/s41598-018-32747-x
Kenyon LJ, Meulia T, Sabree ZL (2015) Habitat visualization and genomic analysis of “Candidatus Pantoea carbekii”, the primary symbiont of the brown marmorated stink bug. Genome Biol Evol 7:620–635. https://doi.org/10.1093/gbe/evv006
Kikuchi Y (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24:195–204. https://doi.org/10.1264/jsme2.me09140s
Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont mediated insecticide resistance. PNAS 109:8618–8622. https://doi.org/10.1073/pnas.1200231109
Kim BR, Shin J, Guevarra RB, Lee JH, Kim DW, Seol KH, Lee JH, Kim HB, Isaacson RE (2017) Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 27:2089–2093. https://doi.org/10.4014/jmb.1709.09027
Kwong WK, Mancenido AL, Moran NA (2017) Immune system stimulation by the native gut microbiota of honey bees. R Soc Open Sci 4:170003. https://doi.org/10.1098/rsos.170003
Lim L, Ab Majid AH (2020) Metagenomic 16S rDNA amplicon data of microbial diversity of guts of fully fed tropical bed bugs, Cimex hemipterus (F.) (Hemiptera: Cimicidae). Data Brief 30:105575. https://doi.org/10.1016/j.dib.2020.105575
Meng L, Li X, Cheng X, Zhang H (2019) 16S rRNA Gene sequencing reveals a shift in the microbiota of Diaphorina citri during the psyllid life cycle. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01948
Moriyama M, Nikoh N, Hosokawa T, Fukatsu T (2015) Riboflavin provisioning underlies Wolbachia’s fitness contribution to its insect host. mBio https://doi.org/10.1128/mbio.01732-15
Moran NA, Tran P, Gerardo NM (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 71(12):8802–8810. https://doi.org/10.1128/AEM.71.12.8802-8810.2005
Muhammad A, Fang Y, Hou Y, Shi Z (2017) The gut entomotype of red palm weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae) and their effect on host nutrition metabolism. Front Microbiol. https://doi.org/10.3389/fmicb.2017.02291
Ojha A, Sinha DK, Padmakumari AP et al (2017) Bacterial community structure in the Asian rice gall midge reveals a varied microbiome rich in Proteobacteria. Sci Rep 7:9424. https://doi.org/10.1038/s41598-017-09791-0
Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. PNAS 100:1803–1807. https://doi.org/10.1073/pnas.0335320100
Pinto-Tomas A, Anderson M, Suen G et al (2009) Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:1120–1123
Ramírez-Puebla ST, Ormeño-Orrillo E, Vera-Ponce de León A, Lozano L, Sanchez-Flores A, Rosenblueth M, Martínez-Romero E (2016) Genomes of Candidatus Wolbachia bourtzisii wDacA and Candidatus Wolbachia pipientis wDacB from the Cochineal Insect Dactylopius coccus (Hemiptera: Dactylopiidae). Genes Genomes Genetics 6:3343–3349. https://doi.org/10.1534/g3.116.031237
Shamim G, Ranjan SK, Kandasamy T, Sharma KK, Ramani R (2017) Bacterial flora associated with Kerria lacca (Kerr). Indian J Entomol 79:41. https://doi.org/10.5958/0974-8172.2017.00010.4
Shamim G, Sharma KK, Ramani R (2019) Isolation and identification of culturable bacteria from honeydew of Indian lac insect, Kerria lacca (Kerr) (Hemiptera: Tachardiidae). Meta Gene 19:10–14. https://doi.org/10.1016/j.mgene.2018.09.010
Siddiqui SA (2004) Lac- The versatile natural resin. Natural Product Radiance 3(5):332–337
Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PloS One 9(8):e105592. https://doi.org/10.1371/journal.pone.0105592
Thamilarasi K, Ekbal S, Gupta M, Kumari K, Lohot VD, Mohanasundaram A, Sharma KK (2018) Plant host induced variation of endosymbionts associated with kusmi lac insects. Multilogic in Science VIII(C) 99–102
Thamilarasi K, Sharma KK (2019) Interaction of lac insects with microbes. In: Kumar A, Kumar N, Chand H (ed). Commercial Entomology. New India Publishing Agency, New Delhi, India (ISBN- 978–93–87973–87–9), pp 129–140
Vashishtha A, Sharama KK, Lakhanpaul S (2011) Co-Existence, phylogeny and putative role of Wolbachia and Yeast-Like Symbiont (YLS) in Kerria lacca (Kerr). Curr Microbiol 63:206–212. https://doi.org/10.1007/s00284-011-9961-x
Walterson AM, Stavrinides J (2015) Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol Rev 39:968–984. https://doi.org/10.1093/femsre/fuv027
Wang Y, Gilbreath TM III, Kukutla P, Yan G, Xu J (2011) Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PloS One 6(9):e24767. https://doi.org/10.1371/journal.pone.0024767
Yong HS, Song SL, Chua KO, Lim PE (2017) High diversity of bacterial communities in developmental stages of Bactrocera carambolae (Insecta: Tephritidae) revealed by Illumina MiSeq Sequencing of 16S rRNA Gene. Curr Microbiol 74(9):1076–1082. https://doi.org/10.1007/s00284-017-1287-x
Yun J, Roh SW, Whon TW et al (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80:5254–5264. https://doi.org/10.1128/AEM.01226-14
Zhao C, Zhao H, Zhang S, Luo J, Zhu X, Wang L, Zhao P, Hua H, Cui J (2019) The developmental stage symbionts of the pea aphid-feeding Chrysoperla sinica (Tjeder). Front Microbiol. https://doi.org/10.3389/fmicb.2019.02454
Zhou J, Duan J, Gao M, Wang Y, Wang X, Zhao K (2018) Diversity, roles, and biotechnological applications of symbiotic microorganisms in the gut of termite. Curr Microbiol 76:755–761. https://doi.org/10.1007/s00284-018-1502-4
Acknowledgements
Authors wish to acknowledge Indian Council of Agricultural Research for providing funds to carry out this work.
Funding
This study was funded by Indian Council of Agricultural Research, New Delhi under Network Project on Conservation of Lac Insect Genetic Resources.
Author information
Authors and Affiliations
Contributions
Thamilarasi Kandasamy conceived the project, analyzed the data and wrote the manuscript; Sajiya Ekbal carried out all wet lab experiments; Kanchan Kumari carried out bioinformatic analyses; Vaibhav D Lohot contributed in maintaining lac insect culture and data analysis, A Mohanasundaram cultured lac insects and provided insect samples used in the experiments, Kewal K Sharma arranged for funding and contributed in refining the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or higher animals performed by any of the authors. Lac insects used in this study are cultured at Institute Research Farm of ICAR-IINRG, Ranchi for research purpose and that there is no need to take any ethical approval.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kandasamy, T., Ekbal, S., Kumari, K. et al. Unraveling bacterial diversity of the Indian Lac Insect Kerria lacca (Kerr) using next generation sequencing. Int J Trop Insect Sci 42, 2365–2372 (2022). https://doi.org/10.1007/s42690-022-00758-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-022-00758-x