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An Insight into Diversity and Functionalities of Gut Microbiota in Insects

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Abstract

The gut microbiota has long been of research interests due to its nutritional importance for many insects. It has been demonstrated that diversity of gut microbiota in insects can be modulated by many factors, including habitats, feeding preference, etc. Besides, the community structure of gut microbiota could also be altered during the different life stages of host insects. With development of conventional culture-dependent technologies and advanced culture-independent technologies, comprehensive and deep understanding of the functions of gut microbiota and their relationship with host insects were achieved, especially for the nutrient metabolic process mediated by them. In this review, we summarized the gut microbiota composition, major methods for gut microbiota characterization, and vital nutrient metabolic process mediated by gut microbiota in different insects. The increasing knowledge on the modulation of gut microbiota will help us for the comprehension of the contribution of gut microbiota to the nutritional metabolism of insects, prompting their growth and health.

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References

  1. Engel P, Moran NA (2013) The gut microbiota of insects-diversity in structure and function. FEMS Microbiol Rev 37(5):699–735. https://doi.org/10.1111/1574-6976.12025

    Article  PubMed  CAS  Google Scholar 

  2. Adak A, Khan MR (2018) An insight into gut microbiota and its functionalities. Cell Mol Life Sci 76(3):473–493. https://doi.org/10.1007/s00018-018-2943-4

    Article  PubMed  CAS  Google Scholar 

  3. Klassen JL (2014) Microbial secondary metabolites and their impacts on insect symbioses. Curr Opin Insect Sci 4:15–22. https://doi.org/10.1016/j.cois.2014.08.004

    Article  PubMed  Google Scholar 

  4. Rohlfs M, Churchill AC (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48(1):23–34. https://doi.org/10.1016/j.fgb.2010.08.008

    Article  PubMed  CAS  Google Scholar 

  5. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37. https://doi.org/10.1146/annurev.ento.43.1.17

    Article  PubMed  CAS  Google Scholar 

  6. Zhang G, Hussain M, O’Neill SL, Asgari S (2013) Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc Natl Acad Sci USA 110(25):10276–10281. https://doi.org/10.1073/pnas.1303603110

    Article  PubMed  Google Scholar 

  7. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34. https://doi.org/10.1146/annurev-ento-010814-020822

    Article  PubMed  CAS  Google Scholar 

  8. Lee JB, Park K-E, Lee SA, Jang SH, Eo HJ, Am Jang H, Kim C-H, Ohbayashi T, Matsuura Y, Kikuchi Y (2017) Gut symbiotic bacteria stimulate insect growth and egg production by modulating hexamerin and vitellogenin gene expression. Dev Comp Immunol 69:12–22. https://doi.org/10.1016/j.dci.2016.11.019

    Article  PubMed  CAS  Google Scholar 

  9. Liao X, Mao K, Ali E, Zhang X, Wan H, Li J (2017) Temporal variability and resistance correlation of sulfoxaflor susceptibility among Chinese populations of the brown planthopper Nilaparvata lugens (Stål). Crop Protect 102:141–146. https://doi.org/10.1016/j.cropro.2017.08.024

    Article  CAS  Google Scholar 

  10. Jones RM, Desai C, Darby TM, Luo L, Wolfarth AA, Scharer CD, Ardita CS, Reedy AR, Keebaugh ES, Neish AS (2015) Lactobacilli modulate epithelial cytoprotection through the Nrf2 pathway. Cell Rep 12(8):1217–1225. https://doi.org/10.1016/j.celrep.2015.07.042

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Broderick NA, Lemaitre B (2012) Gut-associated microbes of Drosophila melanogaster. Gut microbes 3(4):307–321. https://doi.org/10.4161/gmic.19896

    Article  PubMed  PubMed Central  Google Scholar 

  12. Krishnan S, Cooper JA (2014) Effect of dietary fatty acid composition on substrate utilization and body weight maintenance in humans. Eur J Nutr 53(3):691–710. https://doi.org/10.1007/s00394-013-0638-z

    Article  PubMed  CAS  Google Scholar 

  13. Moll RM, Romoser WS, Modrakowski MC, Moncayo AC, Lerdthusnee K (2001) Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol 38(1):29–32. https://doi.org/10.1603/0022-2585-38.1.29

    Article  PubMed  CAS  Google Scholar 

  14. Kaufman MG, Klug MJ, Merritt RW (1989) Growth and food utilization parameters of germ-free house crickets, Acheta domesticus. J Insect Physiol 35(12):957–967. https://doi.org/10.1016/0022-1910(89)90019-X

    Article  Google Scholar 

  15. Kashima T, Nakamura T, Tojo S (2006) Uric acid recycling in the shield bug, Parastrachia japonensis (Hemiptera: Parastrachiidae), during diapause. J Insect Physiol 52(8):816–825. https://doi.org/10.1016/j.jinsphys.2006.05.003

    Article  PubMed  CAS  Google Scholar 

  16. Hongoh Y (2010) Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci Biotechnol Biochem 74(6):1145–1151. https://doi.org/10.1271/bbb.100094

    Article  PubMed  CAS  Google Scholar 

  17. Douglas AE (2018) Omics and the metabolic function of insect-microbial symbioses. Curr Opin Insect Sci 29:1–6. https://doi.org/10.1016/j.cois.2018.05.012

    Article  PubMed  Google Scholar 

  18. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302. https://doi.org/10.1146/annurev.ento.54.110807.090559

    Article  PubMed  CAS  Google Scholar 

  19. Yun J-H, Roh SW, Whon TW, Jung M-J, Kim M-S, Park D-S, Yoon C, Nam Y-D, Kim Y-J, Choi J-H, Kim J-Y, Shin N-R, Kim S-H, Lee W-J, Bae J-W (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80(17):5254–5264. https://doi.org/10.1128/AEM.01226-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. https://doi.org/10.1146/annurev.ento.49.061802.123416

    Article  PubMed  CAS  Google Scholar 

  21. Paniagua Voirol LR, Frago E, Kaltenpoth M, Hilker M, Fatouros NE (2018) Bacterial symbionts in lepidoptera: their diversity, transmission, and impact on the host. Front Microbiol 9:556. https://doi.org/10.3389/fmicb.2018.00556

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hongoh Y, Ekpornprasit L, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Noparatnaraporn N, Kudo T (2006) Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol Ecol 15(2):505–516. https://doi.org/10.1111/j.1365-294X.2005.02795.x

    Article  PubMed  CAS  Google Scholar 

  23. Vargas-Asensio G, Pinto-Tomas A, Rivera B, Hernandez M, Hernandez C, Soto-Montero S, Murillo C, Sherman DH, Tamayo-Castillo G (2014) Uncovering the cultivable microbial diversity of costa rican beetles and its ability to break down plant cell wall components. PLoS ONE 9(11):e113303. https://doi.org/10.1371/journal.pone.0113303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Samoilova ES, Kostina NV, Striganova BR (2016) Microbial population of the digestive tract of click beetle larvae (Elateridae, Coleoptera). Izv Akad Nauk Ser Biol 5:532–543. https://doi.org/10.1134/S1062359016050083

    Article  CAS  Google Scholar 

  25. Lund JB, List M, Baumbach J (2017) Interactive microbial distribution analysis using BioAtlas. Nucleic Acids Res 45(W1):W509–w513. https://doi.org/10.1093/nar/gkx304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Edgar R (2018) Taxonomy annotation and guide tree errors in 16S rRNA databases. PeerJ 6:e5030. https://doi.org/10.7717/peerj.5030

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF, Harrison SP, Kraft NJB, Stegen JC, Swenson NG (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14(1):19–28. https://doi.org/10.1111/j.1461-0248.2010.01552.x

    Article  PubMed  Google Scholar 

  28. Maynard C, Weinkove D (2018) The gut microbiota and ageing. Subcell Biochem 90:351–371. https://doi.org/10.1007/978-981-13-2835-0_12

    Article  PubMed  CAS  Google Scholar 

  29. Clark RI, Salazar A, Yamada R, Fitz-Gibbon S, Morselli M, Alcaraz J, Rana A, Rera M, Pellegrini M, Ja WW, Walker DW (2015) Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep 12(10):1656–1667. https://doi.org/10.1016/j.celrep.2015.08.004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Borrelli L, Coretti L, Dipineto L, Bovera F, Menna F, Chiariotti L, Nizza A, Lembo F, Fioretti A (2017) Insect-based diet, a promising nutritional source, modulates gut microbiota composition and SCFAs production in laying hens. Sci Rep 7(1):16269. https://doi.org/10.1038/s41598-017-16560-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Anderson KE, Ricigliano VA, Mott BM, Copeland DC, Floyd AS, Maes P (2018) The queen's gut refines with age: longevity phenotypes in a social insect model. Microbiome 6(1):108. https://doi.org/10.1186/s40168-018-0489-1

    Article  PubMed  PubMed Central  Google Scholar 

  32. Remolina SC, Hughes KA (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age (Dordr) 30(2–3):177–185. https://doi.org/10.1007/s11357-008-9061-4

    Article  Google Scholar 

  33. Kwong WK, Medina LA, Koch H, Sing K-W, Soh EJY, Ascher JS, Jaffé R, Moran NA (2017) Dynamic microbiome evolution in social bees. Sci Adv 3(3):e1600513. https://doi.org/10.1126/sciadv.1600513

    Article  PubMed  PubMed Central  Google Scholar 

  34. Wang X, Gao Q, Wang W, Wang X, Lei C, Zhu F (2018) The gut bacteria across life stages in the synanthropic fly Chrysomya megacephala. BMC Microbiol 18(1):131. https://doi.org/10.1186/s12866-018-1272-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. McCutcheon JP, Boyd BM, Dale C (2019) The life of an insect endosymbiont from the cradle to the grave. Curr Biol 29(11):R485–r495. https://doi.org/10.1016/j.cub.2019.03.032

    Article  PubMed  CAS  Google Scholar 

  36. Romero S, Nastasa A, Chapman A, Kwong WK, Foster LJ (2019) The honey bee gut microbiota: strategies for study and characterization. Insect Mol Biol 28(4):455–472. https://doi.org/10.1111/imb.12567

    Article  PubMed  CAS  Google Scholar 

  37. Gong J, Yang C (2012) Advances in the methods for studying gut microbiota and their relevance to the research of dietary fiber functions. Food Res Int 48(2):916–929. https://doi.org/10.1016/j.foodres.2011.12.027

    Article  CAS  Google Scholar 

  38. Sarangi AN, Goel A, Aggarwal R (2019) Methods for studying gut microbiota: a primer for physicians. J Clin Exp Hepatol 9(1):62–73. https://doi.org/10.1016/j.jceh.2018.04.016

    Article  PubMed  Google Scholar 

  39. Rouzé R, Moné A, Delbac F, Belzunces L, Blot N (2019) The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae. Microbes Environ 34(3):226–233. https://doi.org/10.1264/jsme2.ME18169

    Article  PubMed  PubMed Central  Google Scholar 

  40. De Palma G, Nadal I, Collado MC, Sanz Y (2009) Effects of a gluten-free diet on gut microbiota and immune function in healthy adult human subjects. Br J Nutr 102(8):1154–1160. https://doi.org/10.1017/S0007114509371767

    Article  PubMed  CAS  Google Scholar 

  41. Ni J, Tokuda G (2013) Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnol Adv 31(6):838–850. https://doi.org/10.1016/j.biotechadv.2013.04.005

    Article  PubMed  CAS  Google Scholar 

  42. Chen MX, Wang S-Y, Kuo C-H, Tsai IL (2019) Metabolome analysis for investigating host-gut microbiota interactions. J Formos Med Assoc 118(Suppl 1):S10–S22. https://doi.org/10.1016/j.jfma.2018.09.007

    Article  PubMed  CAS  Google Scholar 

  43. Ogué-Bon E, Khoo C, McCartney AL, Gibson GR, Rastall RA (2010) In vitro effects of synbiotic fermentation on the canine faecal microbiota. FEMS Microbiol Ecol 73(3):587–600. https://doi.org/10.1111/j.1574-6941.2010.00915.x

    Article  PubMed  CAS  Google Scholar 

  44. Liu N, Zhang L, Zhou H, Zhang M, Yan X, Wang Q, Long Y, Xie L, Wang S, Huang Y, Zhou Z (2013) Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLoS ONE 8(7):e69184. https://doi.org/10.1371/journal.pone.0069184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Savijoki K, Ingmer H, Varmanen P (2006) Proteolytic systems of lactic acid bacteria. Appl Microbiol Biotechnol 71(4):394–406. https://doi.org/10.1007/s00253-006-0427-1

    Article  PubMed  CAS  Google Scholar 

  46. Liu M, Bayjanov JR, Renckens B, Nauta A, Siezen RJ (2010) The proteolytic system of lactic acid bacteria revisited: a genomic comparison. BMC Genomics 11:36. https://doi.org/10.1186/1471-2164-11-36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Pessione E (2012) Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Front Cell Infect Microbiol 2:86. https://doi.org/10.3389/fcimb.2012.00086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Birkle LM, Minto LB, Douglas AE (2002) Relating genotype and phenotype for tryptophan synthesis in an aphid–bacterial symbiosis. Physiol Entomol 27(4):302–306. https://doi.org/10.1046/j.1365-3032.2002.00301.x

    Article  CAS  Google Scholar 

  49. Scully ED, Geib SM, Carlson JE, Tien M, Mckenna DD, Hoover K (2014) Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics 15(1):1096–1096. https://doi.org/10.1186/1471-2164-15-1096

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Ayayee PA, Larsen T, Rosa C, Felton GW, Ferry JG, Hoover K (2016) Essential amino acid supplementation by gut microbes of a wood-feeding cerambycid. Environ Entomol 45(1):66–73. https://doi.org/10.1093/ee/nvv153

    Article  PubMed  CAS  Google Scholar 

  51. Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA (2017) Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci USA 114(18):4775–4780. https://doi.org/10.1073/pnas.1701819114

    Article  PubMed  CAS  Google Scholar 

  52. Ong SY, Kho HP, Riedel SL, Kim SW, Gan CY, Taylor TD, Sudesh K (2018) An integrative study on biologically recovered polyhydroxyalkanoates (PHAs) and simultaneous assessment of gut microbiome in yellow mealworm. J Biotechnol 265:31–39. https://doi.org/10.1016/j.jbiotec.2017.10.017

    Article  PubMed  CAS  Google Scholar 

  53. Shin B, Park SH, Kim B-Y, Jo S-I, Lee SK, Shin J, Oh D-C (2017) Deinococcucins A-D, aminoglycolipids from Deinococcus sp., a gut bacterium of the carpenter ant Camponotus japonicus. J Nat Prod 80(11):2910–2916. https://doi.org/10.1021/acs.jnatprod.7b00426

    Article  PubMed  CAS  Google Scholar 

  54. Anand AA, Vennison SJ, Sankar SG, Prabhu DI, Vasan PT, Raghuraman T, Geoffrey CJ, Vendan SE (2010) Isolation and characterization of bacteria from the gut of Bombyx mori that degrade cellulose, xylan, pectin and starch and their impact on digestion. J Insect Sci 10:107. https://doi.org/10.1673/031.010.10701

    Article  PubMed  PubMed Central  Google Scholar 

  55. Gales A, Chatellard L, Abadie M, Bonnafous A, Auer L, Carrere H, Godon JJ, Hernandez-Raquet G, Dumas C (2018) Screening of phytophagous and xylophagous insects guts microbiota abilities to degrade lignocellulose in bioreactor. Front Microbiol 9:2222. https://doi.org/10.3389/fmicb.2018.02222

    Article  PubMed  PubMed Central  Google Scholar 

  56. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450(7169):560–565. https://doi.org/10.1038/nature06269

    Article  PubMed  CAS  Google Scholar 

  57. Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244(5418):577. https://doi.org/10.1038/244577a0

    Article  PubMed  CAS  Google Scholar 

  58. Benemann JR (1973) Nitrogen fixation in termites. Science 181(4095):164–165. https://doi.org/10.1126/science.181.4095.164

    Article  PubMed  CAS  Google Scholar 

  59. Yamada A, Inoue T, Wiwatwitaya D, Ohkuma M, Kudo T, Sugimoto A (2006) Nitrogen fixation by termites in tropical forests, Thailand. Ecosystem 9(1):75–83. https://doi.org/10.1007/S10021-005-0024-7

    Article  CAS  Google Scholar 

  60. Zhou J, Duan J, Gao M, Wang Y, Wang X, Zhao K (2019) Diversity, roles, and biotechnological applications of symbiotic microorganisms in the gut of termite. Curr Microbiol 76(6):755–761. https://doi.org/10.1007/s00284-018-1502-4

    Article  PubMed  CAS  Google Scholar 

  61. Meuti ME, Jones SC, Curtis PS (2010) 15N discrimination and the sensitivity of nitrogen fixation to changes in dietary nitrogen in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Environ Entomol 39(6):1810–1815. https://doi.org/10.1603/EN10082

    Article  PubMed  Google Scholar 

  62. Shukla SP, Sanders JG, Byrne MJ, Pierce NE (2016) Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae. Mol Ecol 25(24):6092–6106. https://doi.org/10.1111/mec.13901

    Article  PubMed  CAS  Google Scholar 

  63. Salem H, Florez L, Gerardo N, Kaltenpoth M (2015) An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc Biol Sci 282(1804):20142957. https://doi.org/10.1098/rspb.2014.2957

    Article  PubMed  PubMed Central  Google Scholar 

  64. Salem H, Bauer E, Strauss AS, Vogel H, Marz M, Kaltenpoth M (2014) Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc Biol Sci 281(1796):20141838. https://doi.org/10.1098/rspb.2014.1838

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23(1):38–47. https://doi.org/10.1111/j.1365-2435.2008.01442.x

    Article  Google Scholar 

  66. Blow F, Gioti A, Goodhead IB, Kalyva M, Kampouraki A, Vontas J, Darby AC (2020) Functional genomics of a symbiotic community: shared traits in the olive fruit fly gut microbiota. Genome Biol Evol 12(2):3778–3791. https://doi.org/10.1093/gbe/evz258

    Article  PubMed  Google Scholar 

  67. Nakajima H, Hongoh Y, Usami R, Kudo T, Ohkuma M (2005) Spatial distribution of bacterial phylotypes in the gut of the termite Reticulitermes speratus and the bacterial community colonizing the gut epithelium. FEMS Microbiol Ecol 54(2):247–255. https://doi.org/10.1016/j.femsec.2005.03.010

    Article  PubMed  CAS  Google Scholar 

  68. Shinzato N, Muramatsu M, Matsui T, Watanabe Y (2007) Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Odontotermes formosanus. Biosci Biotechnol Biochem 71(4):906–915. https://doi.org/10.1271/bbb.60540

    Article  PubMed  CAS  Google Scholar 

  69. Thongaram T, Hongoh Y, Kosono S, Ohkuma M, Trakulnaleamsai S, Noparatnaraporn N, Kudo T (2005) Comparison of bacterial communities in the alkaline gut segment among various species of higher termites. Extremophiles 9(3):229–238. https://doi.org/10.1007/s00792-005-0440-9

    Article  PubMed  Google Scholar 

  70. Mackenzie LM, Muigai AT, Osir EO, Lwande W, Keller M, Toledo G, Boga HI (2007) Bacterial diversity in the intestinal tract of the funguscultivating termite Macrotermes michaelseni (Sjöstedt). Afr J Biotechnol 6(6):658–667. https://doi.org/10.4314/ajb.v6i6.56873

    Article  CAS  Google Scholar 

  71. Cruden D, Markovetz A (1984) Microbial aspects of the cockroach hindgut. Arch Microbiol 138(2):131–139. https://doi.org/10.1007/bf00413013

    Article  PubMed  CAS  Google Scholar 

  72. Cruden D, Markovetz A (1987) Microbial ecology of the cockroach gut. Annu Rev Microbiol 41(1):617–643. https://doi.org/10.1146/annurev.mi.41.100187.003153

    Article  PubMed  CAS  Google Scholar 

  73. Kakumanu ML, Maritz JM, Carlton JM, Schal C (2018) Overlapping community compositions of gut and fecal microbiomes in lab-reared and field-collected german cockroaches. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01037-18

    Article  PubMed  PubMed Central  Google Scholar 

  74. Garofalo C, Osimani A, Milanović V, Taccari M, Cardinali F, Aquilanti L, Riolo P, Ruschioni S, Isidoro N, Clementi F (2017) The microbiota of marketed processed edible insects as revealed by high-throughput sequencing. Food Microbiol 62:15–22. https://doi.org/10.1016/j.fm.2016.09.012

    Article  PubMed  CAS  Google Scholar 

  75. Waite DWDM, Biswas K, Ward DF, Deines P, Taylor MW (2015) Microbial community structure in the gut of the New Zealand insect Auckland tree weta (Hemideina thoracica). Arch Microbiol 197(4):603–612. https://doi.org/10.1007/s00203-015-1094-3

    Article  PubMed  CAS  Google Scholar 

  76. Jiang CL, Jin WZ, Tao XH, Zhang Q, Zhu J, Feng SY, Xu XH, Li HY, Wang ZH, Zhang ZJ (2019) Black soldier fly larvae (Hermetia illucens) strengthen the metabolic function of food waste biodegradation by gut microbiome. Microb Biotechnol 12(3):528–543. https://doi.org/10.1111/1751-7915.13393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Liu C, Wang C, Yao H (2019) Comprehensive resource utilization of waste using the black soldier fly (Hermetia illucens (L.)) (Diptera: Stratiomyidae). Animals (Basel). https://doi.org/10.3390/ani9060349

    Article  PubMed  PubMed Central  Google Scholar 

  78. Khamesipour F, Lankarani KB, Honarvar B, Kwenti TE (2018) A systematic review of human pathogens carried by the housefly (Musca domestica L.). BMC Public Health 18(1):1049. https://doi.org/10.1186/s12889-018-5934-3

    Article  PubMed  PubMed Central  Google Scholar 

  79. Remolina SC, Hughes KA (2008) Evolution and mechanisms of long life and high fertility in queen honey bees. Age (Dordr) 30(2–3):177–185. https://doi.org/10.1007/s11357-008-9061-4

    Article  Google Scholar 

  80. Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78(8):2830–2840. https://doi.org/10.1128/aem.07810-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Richter MR (2000) Social wasp (Hymenoptera: Vespidae) foraging behavior. Annu Rev Entomol 45:121–150. https://doi.org/10.1146/annurev.ento.45.1.121

    Article  PubMed  CAS  Google Scholar 

  82. Suenami S, Konishi Nobu M, Miyazaki R (2019) Community analysis of gut microbiota in hornets, the largest eusocial wasps, Vespa mandarinia and V. simillima. Sci Rep 9(1):9830. https://doi.org/10.1038/s41598-019-46388-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Grigorescu AS, Renoz F, Sabri A, Foray V, Hance T, Thonart P (2018) Accessing the hidden microbial diversity of aphids: an illustration of how culture-dependent methods can be used to decipher the insect microbiota. Microb Ecol 75(4):1035–1048. https://doi.org/10.1007/s00248-017-1092-x

    Article  PubMed  Google Scholar 

  84. Vivero RJ, Jaramillo NG, Cadavid-Restrepo G, Soto SI, Herrera CX (2016) Structural differences in gut bacteria communities in developmental stages of natural populations of Lutzomyia evansi from Colombia's Caribbean coast. Parasit Vectors 9:496. https://doi.org/10.1186/s13071-016-1766-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Lagier JC, Khelaifia S, Alou MT et al (2016) Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol 1:16203. https://doi.org/10.1038/nmicrobiol.2016.203

    Article  PubMed  CAS  Google Scholar 

  86. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA, Stares MD, Goulding D, Lawley TD (2016) Culturing of 'unculturable' human microbiota reveals novel taxa and extensive sporulation. Nature 533(7604):543–546. https://doi.org/10.1038/nature17645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Lagier JC, Hugon P, Khelaifia S, Fournier PE, La Scola B, Raoult D (2015) The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin Microbiol Rev 28(1):237–264. https://doi.org/10.1128/cmr.00014-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Lau JT, Whelan FJ, Herath I, Lee CH, Collins SM, Bercik P, Surette MG (2016) Capturing the diversity of the human gut microbiota through culture-enriched molecular profiling. Genome Med 8(1):72. https://doi.org/10.1186/s13073-016-0327-7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Costes B, Girodon E, Ghanem N, Chassignol M, Thuong NT, Dupret D, Goossens M (1993) Psoralen-modified oligonucleotide primers improve detection of mutations by denaturing gradient gel electrophoresis and provide an alternative to GC-clamping. Hum Mol Genet 2(4):393–397. https://doi.org/10.1093/hmg/2.4.393

    Article  PubMed  CAS  Google Scholar 

  90. Wang Y, Hammes F, De Roy K, Verstraete W, Boon N (2010) Past, present and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol 28(8):416–424. https://doi.org/10.1016/j.tibtech.2010.04.006

    Article  PubMed  CAS  Google Scholar 

  91. Metzker ML (2005) Emerging technologies in DNA sequencing. Genome Res 15(12):1767–1776. https://doi.org/10.1101/gr.3770505

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Key Technology R & D Program of China (2018YFD0500203 to LY, CY, and 2018YFD0500204 to LF). LY and CY also acknowledge the support from State Key Laboratory of Biocatalysis and Enzyme Engineering.

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Conceptualization: SW, LY; Investigation: SW, LW, XF, CY; Writing-original draft preparation: SW; Formal analysis: LY, LF.

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Correspondence to Li Yi.

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Wang, S., Wang, L., Fan, X. et al. An Insight into Diversity and Functionalities of Gut Microbiota in Insects. Curr Microbiol 77, 1976–1986 (2020). https://doi.org/10.1007/s00284-020-02084-2

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