1932

Abstract

Bacteriocytes are host cells specialized to harbor symbionts in certain insect taxa. The adaptation, development, and evolution of bacteriocytes underlie insect symbiosis maintenance. Bacteriocytes carry enriched host genes of insect and bacterial origin whose transcription can be regulated by microRNAs, which are involved in host–symbiont metabolic interactions. Recognition proteins of peptidoglycan, the bacterial cell wall component, and autophagy regulate symbiont abundance in bacteriocytes. Horizontally transferred genes expressed in bacteriocytes influence the metabolism of symbiont peptidoglycan, which may affect the bacteriocyte immune response against symbionts. Bacteriocytes release or transport symbionts into ovaries for symbiont vertical transmission. Bacteriocyte development and death, regulated by transcriptional factors, are variable in different insect species. The evolutionary origin of insect bacteriocytes remains unclear. Future research should elucidate bacteriocyte cell biology, the molecular interplay between bacteriocyte metabolic and immune functions, the genetic basis of bacteriocyte origin, and the coordination between bacteriocyte function and host biology in diverse symbioses.

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2024-01-25
2024-12-13
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Literature Cited

  1. 1.
    Anselme C, Vallier A, Balmand S, Fauvarque MO, Heddi A. 2006. Host PGRP gene expression and bacterial release in endosymbiosis of the weevil Sitophilus zeamais. Appl. Environ. Microbiol. 72:6766–72
    [Google Scholar]
  2. 2.
    Bao XY, Yan JY, Yao YL, Wang YB, Visendi P et al. 2021. Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts. PLOS Pathog 17:e1010120
    [Google Scholar]
  3. 3.
    Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155–89
    [Google Scholar]
  4. 4.
    Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S et al. 2003. Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLOS Biol 1:e21
    [Google Scholar]
  5. 5.
    Bressan A, Arneodo J, Simonato M, Haines WP, Boudon-Padieu E. 2009. Characterization and evolution of two bacteriome-inhabiting symbionts in cixiid planthoppers (Hemiptera: Fulgoromorpha: Pentastirini). Environ. Microbiol. 11:3265–79
    [Google Scholar]
  6. 6.
    Bressan A, Mulligan KL. 2013. Localization and morphological variation of three bacteriome-inhabiting symbionts within a planthopper of the genus Oliarus (Hemiptera: Cixiidae). Environ. Microbiol. Rep. 5:499–505
    [Google Scholar]
  7. 7.
    Bublitz DC, Chadwick GL, Magyar JS, Sandoz KM, Brooks DM et al. 2019. Peptidoglycan production by an insect-bacterial mosaic. Cell 179:703–12
    [Google Scholar]
  8. 8.
    Buchner P. 1965. Endosymbiosis of Animals with Plant Microorganisms Hoboken, NJ: Wiley
    [Google Scholar]
  9. 9.
    Calderon O, Berkov A. 2012. Midgut and fat body bacteriocytes in neotropical cerambycid beetles (Coleoptera: Cerambycidae). Environ. Entomol. 41:108–17
    [Google Scholar]
  10. 10.
    Chu H, Mazmanian SK. 2013. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immun. 14:668–75
    [Google Scholar]
  11. 11.
    Chung SH, Jing X, Luo Y, Douglas AE. 2018. Targeting symbiosis-related insect genes by RNAi in the pea aphid-Buchnera symbiosis. Insect Biochem. Mol. Biol. 95:55–63
    [Google Scholar]
  12. 12.
    Dan H, Ikeda N, Fujikami M, Nakabachi A. 2017. Behavior of bacteriome symbionts during transovarial transmission and development of the Asian citrus psyllid. PLOS ONE 12:e0189779
    [Google Scholar]
  13. 13.
    Dirks U, Gruber-Vodicka HR, Leisch N, Bulgheresi S, Egger B et al. 2012. Bacterial symbiosis maintenance in the asexually reproducing and regenerating flatworm Paracatenula galateia. PLOS ONE 7:e34709
    [Google Scholar]
  14. 14.
    Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43:17–37
    [Google Scholar]
  15. 15.
    Douglas AE. 2014. The molecular basis of bacterial–insect symbiosis. J. Mol. Biol. 426:3830–37
    [Google Scholar]
  16. 16.
    Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34
    [Google Scholar]
  17. 17.
    Douglas AE. 2016. How multi-partner endosymbioses function. Nat. Rev. Microbiol. 14:731–43
    [Google Scholar]
  18. 18.
    Douglas AE. 2020. Housing microbial symbionts: evolutionary origins and diversification of symbiotic organs in animals. Philos. Trans. R. Soc. Lond. B 375:20190603
    [Google Scholar]
  19. 19.
    Douglas AE, Dixon AFG. 1987. The mycetocyte symbiosis of aphids: variation with age and morph in virginoparae of Megoura viciae and Acyrthosiphon pisum. J. Insect Physiol. 33:109–13
    [Google Scholar]
  20. 20.
    Ebert D. 2013. The epidemiology and evolution of symbionts with mixed-mode transmission. Annu. Rev. Ecol. Evol. Syst. 44:623–43
    [Google Scholar]
  21. 21.
    Feng HL, Wang LY, Wuchty S, Wilson ACC. 2018. MicroRNA regulation in an ancient obligate endosymbiosis. Mol. Ecol. 27:1777–93
    [Google Scholar]
  22. 22.
    Filip H, Vaclav H, Alistair D. 2020. Insect-symbiont gene expression in the midgut bacteriocytes of a blood-sucking parasite. Genome Biol. Evol. 12:429–42
    [Google Scholar]
  23. 23.
    Fukatsu T. 2021. The long and winding road for symbiont and yolk protein to host oocyte. mBio 12:e02997-20
    [Google Scholar]
  24. 24.
    Fukumori K, Oguchi K, Ikeda H, Shinohara T, Tanahashi M et al. 2022. Evolutionary dynamics of host organs for microbial symbiosis in tortoise leaf beetles (Coleoptera: Chrysomelidae: Cassidinae). mBio 13:e0369121
    [Google Scholar]
  25. 25.
    Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F et al. 2008. Inherited intracellular ecosystem: Symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22:2591–99
    [Google Scholar]
  26. 26.
    Hadfield SJ, Axton JM. 1999. Germ cells colonized by endosymbiotic bacteria. Nature 402:482
    [Google Scholar]
  27. 27.
    Hammer T, Moran NA. 2019. Links between metamorphosis and symbiosis in holometabolous insects. Philos. Trans. R. Soc. Lond. B 374:20190068
    [Google Scholar]
  28. 28.
    Hansen AK, Moran NA. 2011. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. PNAS 108:2849–54
    [Google Scholar]
  29. 29.
    He C, Klionsky DJ. 2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43:67–93
    [Google Scholar]
  30. 30.
    Herren JK, Paredes JC, Schüpfer F, Lemaitre B. 2013. Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. mBio 4:e00532-12
    [Google Scholar]
  31. 31.
    Hirota B, Meng XY, Fukatsu T. 2020. Bacteriome-associated endosymbiotic bacteria of Nosodendron tree sap beetles (Coleoptera: Nosodendridae). Front. Microbiol. 11:588841
    [Google Scholar]
  32. 32.
    Hirota B, Okude G, Anbutsu H, Futahashi R, Moriyama M et al. 2017. A novel, extremely elongated, and endocellular bacterial symbiont supports cuticle formation of a grain pest beetle. mBio 8:e01482-17
    [Google Scholar]
  33. 33.
    Horak RD, Leonard SP, Moran NA. 2020. Symbionts shape host innate immunity in honeybees. Proc. Biol. Sci. 287:20201184
    [Google Scholar]
  34. 34.
    Husnik F, McCutcheon JP. 2016. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. PNAS 113:E5416–24
    [Google Scholar]
  35. 35.
    Husnik F, McCutcheon JP. 2018. Functional horizontal gene transfer from bacteria to eukaryotes. Nat. Rev. Microbiol. 16:67–79
    [Google Scholar]
  36. 36.
    Husnik F, Nikoh N, Koga R, Ross L, Duncan RP et al. 2013. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153:1567–78
    [Google Scholar]
  37. 37.
    Kaltenpoth M. 2020. An endosymbiont's journey through metamorphosis of its insect host. PNAS 117:202014598
    [Google Scholar]
  38. 38.
    Kikuchi Y. 2009. Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24:195–204
    [Google Scholar]
  39. 39.
    Kim D, Thairu MW, Hansen AK. 2016. Novel insights into insect-microbe interactions-role of epigenomics and small RNAs. Front. Plant Sci. 7:1164
    [Google Scholar]
  40. 40.
    Kim VN, Han J, Siomi MC. 2009. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10:126–39
    [Google Scholar]
  41. 41.
    Kobiałka M, Michalik A, Szwedo J, Szklarzewicz T. 2018. Diversity of symbiotic microbiota in Deltocephalinae leafhoppers (Insecta, Hemiptera, Cicadellidae). Arthropod Struct. Dev. 47:268–78
    [Google Scholar]
  42. 42.
    Koga R, Bennett GM, Cryan JR, Moran NA. 2013. Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 15:2073–81
    [Google Scholar]
  43. 43.
    Koga R, Meng XY, Tsuchida T, Fukatsu T. 2012. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. PNAS 109:E1230–37
    [Google Scholar]
  44. 44.
    Koga R, Nikoh N, Matsuura Y, Meng XY, Fukatsu T. 2013. Mealybugs with distinct endosymbiotic systems living on the same host plant. FEMS Microbiol. Ecol. 83:93–100
    [Google Scholar]
  45. 45.
    Kuechler SM, Fukatsu T, Yu M. 2019. Repeated evolution of bacteriocytes in lygaeoid stinkbugs. Environ. Microbiol. 21:4378–94
    [Google Scholar]
  46. 46.
    Li NN, Jiang S, Lu KY, Hong JS, Wang YB et al. 2022. Bacteriocyte development is sexually differentiated in Bemisia tabaci. Cell Rep 38:110455
    [Google Scholar]
  47. 47.
    Login FH, Balmand S, Vallier A, Vincent-Monegat C, Vigneron A et al. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334:362–65
    [Google Scholar]
  48. 48.
    Luan JB, Chen WB, Hasegawa DK, Simmons AM, Wintermantel WM et al. 2015. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol. Evol. 7:2635–47
    [Google Scholar]
  49. 49.
    Luan JB, Shan HW, Isermann P, Huang JH, Lammerding J et al. 2016. Cellular and molecular remodeling of a host cell for vertical transmission of bacterial symbionts. Proc. R. Soc. Lond. B 283:20160580
    [Google Scholar]
  50. 50.
    Luan JB, Sun XP, Fei Z, Douglas AE. 2018. Maternal inheritance of a single somatic animal cell displayed by the bacteriocyte in the whitefly Bemisia tabaci. Curr. Biol 28:459–65
    [Google Scholar]
  51. 51.
    Łukasik P, Nazario K, Van Leuven JT, Campbell MA, Meyer M et al. 2018. Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas. PNAS 115:E226–35
    [Google Scholar]
  52. 52.
    Macdonald SJ, Lin GG, Russell CW, Thomas GH, Douglas AE. 2012. The central role of the host cell in symbiotic nitrogen metabolism. Proc. Biol. Sci. 279:2965–73
    [Google Scholar]
  53. 53.
    Maire J, Parisot N, Ferrarinia MG, Valliera A, Gillet B et al. 2020. Spatial and morphological reorganization of endosymbiosis during metamorphosis accommodates adult metabolic requirements in a weevil. PNAS 117:19347–58
    [Google Scholar]
  54. 54.
    Maire J, Vincent-Monégat C, Balmand S, Vallier A, Hervé M et al. 2019. Weevil pgrp-lb prevents endosymbiont tct dissemination and chronic host systemic immune activation. PNAS 116:5623–32
    [Google Scholar]
  55. 55.
    Mao M, Bennett GM. 2020. Symbiont replacements reset the co-evolutionary relationship between insects and their heritable bacteria. ISME J 14:1384–95
    [Google Scholar]
  56. 56.
    Mao M, Yang X, Bennett GM. 2018. Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host. PNAS 115:e11691–700
    [Google Scholar]
  57. 57.
    Masson F, Zaidman-Rémy A, Heddi A. 2016. Antimicrobial peptides and cell processes tracking endosymbiont dynamics. Philos. Trans. R. Soc. B 371:20150298
    [Google Scholar]
  58. 58.
    Matsuura Y, Kikuchi Y, Miura T, Fukatsu T. 2015. Ultrabithorax is essential for bacteriocyte development. PNAS 112:9376–81
    [Google Scholar]
  59. 59.
    McCutcheon JP. 2021. The genomics and cell biology of host-beneficial intracellular infections. Annu. Rev. Cell Dev. Biol. 37:115–42
    [Google Scholar]
  60. 60.
    McCutcheon JP, Boyd BM, Dale C. 2019. The life of an insect endosymbiont from the cradle to the grave. Curr. Biol. 29:R485–95
    [Google Scholar]
  61. 61.
    McCutcheon JP, Von Dohlen CD. 2011. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21:1366–72
    [Google Scholar]
  62. 62.
    Medzhitov R, Janeway CA. 2002. Decoding the patterns of self and nonself by the innate immune system. Science 296:298–300
    [Google Scholar]
  63. 63.
    Michalik A, Castillo FD, Kobiałka M, Szklarzewicz T, Stroinski A et al. 2021. Alternative transmission patterns in independently acquired nutritional cosymbionts of Dictyopharidae planthoppers. mBio 12:e01228-21
    [Google Scholar]
  64. 64.
    Michalik A, Michalik K, Grzywacz B, Kalandyk-Kołodziejczyk M, Szklarzewicz T. 2019. Molecular characterization, ultrastructure, and transovarial transmission of Tremblaya phenacola in six mealybugs of the Phenacoccinae subfamily (Insecta, Hemiptera, Coccomorpha). Protoplasma 256:1597–608
    [Google Scholar]
  65. 65.
    Michalik A, Schulz F, Michalik K, Wascher F, Horn M et al. 2018. Coexistence of novel gammaproteobacterial and Arsenophonus symbionts in the scale insect Greenisca brachypodii (Hemiptera, Coccomorpha: Eriococcidae). Environ. Microbiol. 20:1148–57
    [Google Scholar]
  66. 66.
    Michalik A, Szwedo J, Stroinski A, Swierczewski D, Szklarzewicz T. 2018. Symbiotic cornucopia of the monophagous planthopper Ommatidiotus dissimilis (Fallén, 1806) (Hemiptera: Fulgoromorpha: Caliscelidae). Protoplasma 255:1317–29
    [Google Scholar]
  67. 67.
    Michalik K, Szklarzewicz T, Kalandyk-Kołodziejczyk M, Jankowska W, Michalik A. 2016. Bacteria belonging to the genus Burkholderia are obligatory symbionts of the eriococcids Acanthococcus aceris Signoret, 1875 and Gossyparia spuria (Modeer, 1778) (Insecta, Hemiptera, Coccoidea). Arthropod Struct. Dev. 45:265–72
    [Google Scholar]
  68. 68.
    Moran NA, Bennett GM. 2014. The tiniest tiny genomes. Annu. Rev. Microbiol. 68:195–215
    [Google Scholar]
  69. 69.
    Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165–90
    [Google Scholar]
  70. 70.
    Nakabachi A, Koshikawa S, Miura T, Miyagishima S. 2010. Genome size of Pachypsylla venusta (Hemiptera: Psyllidae) and the ploidy of its bacteriocyte, the symbiotic host cell that harbors intracellular mutualistic bacteria with the smallest cellular genome. Bull. Entomol. Res. 100:27–33
    [Google Scholar]
  71. 71.
    Nakabachi A, Shigenobu S, Sakazume N, Shiraki T, Hayashizaki Y et al. 2005. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. PNAS 102:5477–82
    [Google Scholar]
  72. 72.
    Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A et al. 2013. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23:1478–84
    [Google Scholar]
  73. 73.
    Nichols HL, Goldstein EB, Saleh Ziabari O, Parker BJ. 2021. Intraspecific variation in immune gene expression and heritable symbiont density. PLOS Pathog 17:e1009552
    [Google Scholar]
  74. 74.
    Nikoh N, McCutcheon JP, Kudo T, Miyagishima S, Moran NA et al. 2010. Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLOS Genet 6:e1000827
    [Google Scholar]
  75. 75.
    Nikoh N, Nakabachi A. 2009. Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 7:12
    [Google Scholar]
  76. 76.
    Noda T, Okude G, Meng XY, Koga R, Moriyama M et al. 2020. Bacteriocytes and Blattabacterium endosymbionts of the German cockroach Blattella germanica, the forest cockroach Blattella nipponica, and other cockroach species. Zool. Sci. 37:399–410
    [Google Scholar]
  77. 77.
    Nozaki T, Shigenobu S. 2022. Ploidy dynamics in aphid host cells harboring bacterial symbionts. Sci. Rep. 12:9111
    [Google Scholar]
  78. 78.
    Ote M, Yamamoto D. 2020. Impact of Wolbachia infection on Drosophila female germline stem cells. Curr. Opin. Insect Sci. 37:8–15
    [Google Scholar]
  79. 79.
    Pan X, Pike A, Joshi D, Bian G, McFadden MJ et al. 2018. The bacterium Wolbachia exploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquito Aedes aegypti. ISME J 12:277–88
    [Google Scholar]
  80. 80.
    Perlmutter JI, Bordenstein SR. 2020. Microorganisms in the reproductive tissues of arthropods. Nat. Rev. Microbiol. 18:97–111
    [Google Scholar]
  81. 81.
    Perreau J, Moran NA. 2022. Genetic innovations in animal-microbe symbioses. Nat. Rev. Genet. 23:23–39
    [Google Scholar]
  82. 82.
    Pineda-Mendoza RM, Zúñiga G, López MF, Hidalgo-Lara ME, Santiago-Hernández A et al. 2022. Rahnella sp., a dominant symbiont of the core gut bacteriome of Dendroctonus species, has metabolic capacity to degrade xylan by bifunctional xylanase-ferulic acid esterase. Front. Microbiol. 13:911269
    [Google Scholar]
  83. 83.
    Poliakov A, Russell CW, Ponnala L, Hoops HJ, Sun Q et al. 2011. Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Mol. Cell Proteom. 10:M110.007039
    [Google Scholar]
  84. 84.
    Price DRG, Duncan RP, Shigenobu S, Wilson AC. 2011. Genome expansion and differential expression of amino acid transporters at the aphid/Buchnera symbiotic interface. Mol. Biol. Evol. 28:3113–26
    [Google Scholar]
  85. 85.
    Price DRG, Feng H, Baker JD, Bavan S, Luetje CW et al. 2014. Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. PNAS 111:320–25
    [Google Scholar]
  86. 86.
    Rafqi AM, Rajakumar A, Abouheif E. 2020. Origin and elaboration of a major evolutionary transition in individuality. Nature 585:239–44
    [Google Scholar]
  87. 87.
    Ren FR, Sun X, Wang TY, Yan JY, Yao YL et al. 2021. Pantothenate mediates the coordination of whitefly and symbiont fitness. ISME J 15:1655–67
    [Google Scholar]
  88. 88.
    Ren FR, Sun X, Wang TY, Yao YL, Huang YZ et al. 2020. Biotin provisioning by horizontally transferred genes from bacteria confers animal fitness benefits. ISME J 14:2542–53
    [Google Scholar]
  89. 89.
    Renoz F, Lopes MR, Gaget K, Duport G, Eloy MC et al. 2022. Compartmentalized into bacteriocytes but highly invasive: the puzzling case of the co-obligate symbiont Serratia symbiotica in the aphid Periphyllus lyropictus. Microbiol. Spectr. 10:e0045722
    [Google Scholar]
  90. 90.
    Rio R, Attardo GM, Weiss BL. 2016. Grandeur alliances: symbiont metabolic integration and obligate arthropod hematophagy. Trends Parasitol 32:739–49
    [Google Scholar]
  91. 91.
    Royet J, Dziarski R. 2007. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat. Rev. Microbiol. 5:264–77
    [Google Scholar]
  92. 92.
    Royet J, Gupta D, Dziarski R. 2011. Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat. Rev. Immunol. 11:837–51
    [Google Scholar]
  93. 93.
    Russell SL, Chappell L, Sullivan W. 2019. A symbiont's guide to the germline. Curr. Top. Dev. Biol. 135:315–51
    [Google Scholar]
  94. 94.
    Sacchi L, Nalepa CA, Lenz M, Bandi C, Corona S et al. 2000. Transovarial transmission of symbiotic bacteria in Mastotermes darwiniensis (Isoptera: Mastotermitidae): ultrastructural aspects and phylogenetic implications. Ann. Entomol. Soc. Am 6:1308–13
    [Google Scholar]
  95. 95.
    Santos-Garcia D, Mestre-Rincon N, Ouvrard D, Zchori-Fein E, Morin S. 2020. Portiera gets wild: Genome instability provides insights into the evolution of both whiteflies and their endosymbionts. Genome Biol. Evol. 12:2107–24
    [Google Scholar]
  96. 96.
    Schrader F. 1923. The origin of the mycetocytes in Pseudococcus. Biol. Bull. 45:279–302
    [Google Scholar]
  97. 97.
    Serbus LR, Sullivan W. 2007. A cellular basis for Wolbachia recruitment to the host germline. PLOS Pathog 3:e190
    [Google Scholar]
  98. 98.
    Shan HW, Liu YQ, Luan JB, Liu SS. 2021. New insight into the transovarial transmission of the symbiont Rickettsia in whitefly. Sci. China Life Sci. 64:1174–86
    [Google Scholar]
  99. 99.
    Shigenobu S, Wilson A. 2011. Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cell Mol. Life Sci. 68:1297–309
    [Google Scholar]
  100. 100.
    Simonet P, Duport G, Gaget K, Weiss-Gayet M, Colella S et al. 2016. Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Sci. Rep. 6:19967
    [Google Scholar]
  101. 101.
    Simonet P, Gaget K, Balmand S, Lopes MR, Parisot N et al. 2018. Bacteriocyte cell death in the pea aphid/Buchnera symbiotic system. PNAS 115:E1819–28
    [Google Scholar]
  102. 102.
    Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M. 2010. Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol 10:142
    [Google Scholar]
  103. 103.
    Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC et al. 2014. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol. 31:857–71
    [Google Scholar]
  104. 104.
    Smith TE, Lee M, Person MD, Hesek D, Mobashery S et al. 2021. Horizontal-acquisition of a promiscuous peptidoglycan-recycling enzyme enables aphids to influence symbiont cell wall metabolism. mBio 12:e0263621
    [Google Scholar]
  105. 105.
    Smith TE, Li Y, Perreau J, Moran NA. 2022. Elucidation of host and symbiont contributions to peptidoglycan metabolism based on comparative genomics of eight aphid subfamilies and their Buchnera. PLOS Genet 18:e1010195
    [Google Scholar]
  106. 106.
    Stoll S, Feldhaar H, Gross FR. 2010. Bacteriocyte dynamics during development of a holometabolous insect, the carpenter ant Camponotus floridanus. BMC Microbiol 10:308
    [Google Scholar]
  107. 107.
    Sun X, Liu BQ, Chen ZB, Li CQ, Li XY et al. 2023. Vitellogenin facilitates associations between whitefly and a bacteriocyte symbiont. mBio 14:e0299022
    [Google Scholar]
  108. 108.
    Sun X, Liu BQ, Li CQ, Chen ZB, Xu XR et al. 2022. A novel microRNA regulates cooperation between symbionts and a laterally acquired gene in the regulation of pantothenate biosynthesis within Bemisia tabaci whiteflies. Mol. Ecol. 31:2611–24
    [Google Scholar]
  109. 109.
    Szklarzewicz T, Kalandyk-Kołodziejczyk M, Michalik A. 2022. Ovary structure and symbiotic associates of a ground mealybug, Rhizoecus albidus (Hemiptera, Coccomorpha: Rhizoecidae) and their phylogenetic implications. J. Anat. 241:860–72
    [Google Scholar]
  110. 110.
    Szklarzewicz T, Kalandyk-Kołodziejczyk M, Michalik K, Jankowska W, Michalik A. 2018. Symbiotic microorganisms in Puto superbus (Leonardi, 1907) (Insecta, Hemiptera, Coccomorpha: Putoidae). Protoplasma 255:129–38
    [Google Scholar]
  111. 111.
    Szklarzewicz T, Swierczewski D, Stroinski A, Michalik A. 2020. Conservatism and stability of the symbiotic system of the invasive alien treehopper Stictocephala bisonia (Hemiptera, Cicadomorpha, Membracidae). Ecol. Entomol. 45:876–85
    [Google Scholar]
  112. 112.
    Thomas GH, Zucker J, Macdonald SJ, Sorokin A, Goryanin I et al. 2009. A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola. BMC Syst. Biol. 3:24
    [Google Scholar]
  113. 113.
    Toenshoff ER, Gruber D, Horn M. 2012. Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ. Microbiol. 14:1284–95
    [Google Scholar]
  114. 114.
    Toenshoff ER, Penz T, Narzt T, Collingro A, Schmitz-Esser S et al. 2011. Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae). ISME J 6:384–96
    [Google Scholar]
  115. 115.
    Toenshoff ER, Szabo G, Gruber D, Horn M. 2014. The pine bark adelgid, Pineus strobi, contains two novel bacteriocyte-associated gammaproteobacterial symbionts. Appl. Environ. Microbiol. 80:878–85
    [Google Scholar]
  116. 116.
    Tomizawa M, Nakamura Y, Suetsugu Y, Noda H. 2020. Numerous peptidoglycan recognition protein genes expressed in the bacteriome of the green rice leafhopper Nephotettix cincticeps (Hemiptera, Cicadellidae). Appl. Entomol. Zool. 55:259–69
    [Google Scholar]
  117. 117.
    Tufail M, Takeda M. 2008. Molecular characteristics of insect vitellogenins. J. Insect Physiol. 54:1447–58
    [Google Scholar]
  118. 118.
    Uchi N, Fukudome M, Nozaki N, Suzuki M, Osuki KI et al. 2019. Antimicrobial activities of cysteine-rich peptides specific to bacteriocytes of the pea aphid Acyrthosiphon pisum. Microbes Environ 34:155–60
    [Google Scholar]
  119. 119.
    Vanzo N, Oprins A, Xanthakis D, Ephrussi A, Rabouille C. 2007. Stimulation of endocytosis and actin dynamics by Oskar polarizes the Drosophila oocyte. Dev. Cell 12:543–55
    [Google Scholar]
  120. 120.
    Vigneron A, Masson F, Vallier A, Balmand S, Rey M et al. 2014. Insects recycle endosymbionts when the benefit is over. Curr. Biol. 24:2267–73
    [Google Scholar]
  121. 121.
    von Dohlen CD, Kohler S, Alsop ST, McManus WR. 2001. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 412:433–35
    [Google Scholar]
  122. 122.
    Voronin D, Cook DA, Steven A, Taylor MJ. 2012. Autophagy regulates Wolbachia populations across diverse symbiotic associations. PNAS 109:e1638–46
    [Google Scholar]
  123. 123.
    Wang DD, Huang Z, Billen J, Zhang GY, He H, Wei C. 2021. Structural diversity of symbionts and related cellular mechanisms underlying vertical symbiont transmission in cicadas. Environ. Microbiol. 23:6603–21
    [Google Scholar]
  124. 124.
    Wang JW, Aksoy S. 2012. PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse's offspring. PNAS 109:10552–57
    [Google Scholar]
  125. 125.
    Wang JW, Wu Y, Yang G, Aksoy S. 2009. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. PNAS 106:12133–38
    [Google Scholar]
  126. 126.
    Wang TY, Luan JB. 2022. Silencing horizontally transferred genes for the control of the whitefly Bemisia tabaci. J. Pest Sci. 96:195–208
    [Google Scholar]
  127. 127.
    Wang YB, Li C, Yan JY, Wang TY, Yao YL et al. 2022. Autophagy regulates whitefly-symbiont metabolic interactions. Appl. Environ. Microbiol. 88:e0208921
    [Google Scholar]
  128. 128.
    Wang YB, Ren FR, Yao YL, Sun X, Walling LL et al. 2020. Intracellular symbionts drive sex ratio in the whitefly by facilitating fertilization and provisioning of B vitamins. ISME J 14:2923–35
    [Google Scholar]
  129. 129.
    Wilson ACC, Duncan RP. 2015. Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses. PNAS 112:10255–61
    [Google Scholar]
  130. 130.
    Xu XR, Li NN, Bao XY, Douglas AE, Luan JB. 2020. Patterns of host cell inheritance in the bacterial symbiosis of whiteflies. Insect Sci 27:938–46
    [Google Scholar]
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