1932

Abstract

Microbes gain access to eukaryotic cells as food for bacteria-grazing protists, for host protection by microbe-killing immune cells, or for microbial benefit when pathogens enter host cells to replicate. But microbes can also gain access to a host cell and become an important—often required—beneficial partner. The oldest beneficial microbial infections are the ancient eukaryotic organelles now called the mitochondrion and plastid. But numerous other host-beneficial intracellular infections occur throughout eukaryotes. Here I review the genomics and cell biology of these interactions with a focus on intracellular bacteria. The genomes of host-beneficial intracellular bacteria have features that span a previously unfilled gap between pathogens and organelles. Host cell adaptations to allow the intracellular persistence of beneficial bacteria are found along with evidence for the microbial manipulation of host cells, but the cellular mechanisms of beneficial bacterial infections are not well understood.

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2021-10-06
2024-10-07
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Literature Cited

  1. Abby SS, Rocha EPC. 2012. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLOS Genet 8:9e1002983
    [Google Scholar]
  2. Alix E, Mukherjee S, Roy CR 2011. Subversion of membrane transport pathways by vacuolar pathogens. J. Cell Biol. 195:6943–52
    [Google Scholar]
  3. Alvarez M, Casadevall A. 2006. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16:212161–65
    [Google Scholar]
  4. Anand I, Choi W, Isberg RR. 2020. The vacuole guard hypothesis: how intravacuolar pathogens fight to maintain the integrity of their beloved home. Curr. Opin. Microbiol. 54:51–58
    [Google Scholar]
  5. Archibald J. 2014. One Plus One Equals One: Symbiosis and the Evolution of Complex Life Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  6. Barker J, Brown MR. 1994. Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140:Part 61253–59
    [Google Scholar]
  7. Batut B, Knibbe C, Marais G, Daubin V. 2014. Reductive genome evolution at both ends of the bacterial population size spectrum. Nat. Rev. Microbiol. 12:12841–50
    [Google Scholar]
  8. Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155–89
    [Google Scholar]
  9. Baumann P, Baumann L, Lai CY, Rouhbakhsh D, Moran NA, Clark MA. 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:55–94
    [Google Scholar]
  10. Baumann P, Moran NA, Baumann L 2006. Bacteriocyte-associated endosymbionts of insects. In The Prokaryotes, Vol. 1: Symbiotic Associations, Biotechnology, Applied Microbiologyed. M Dworkin, S Falkow, E Rosenberg, KH Schleifer, E Stackebrandt40338 New York: Springer, 3rd ed..
    [Google Scholar]
  11. Bengoechea JA, Sa Pessoa J 2019. Klebsiella pneumoniae infection biology: living to counteract host defences. FEMS Microbiol. Rev. 43:2123–44
    [Google Scholar]
  12. Bhattacharya D, Price DC, Yoon HS, Yang EC, Poulton NJ et al. 2012. Single cell genome analysis supports a link between phagotrophy and primary plastid endosymbiosis. Sci. Rep. 2:356
    [Google Scholar]
  13. Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P. 1996. An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl. Environ. Microbiol. 62:83005–10
    [Google Scholar]
  14. Booth A, Doolittle WF 2015. Eukaryogenesis, how special really?. PNAS 112:3310278–85
    [Google Scholar]
  15. Boulais J, Trost M, Landry CR, Dieckmann R, Levy ED et al. 2010. Molecular characterization of the evolution of phagosomes. Mol. Syst. Biol. 6:423
    [Google Scholar]
  16. Bozzaro S, Bucci C, Steinert M. 2008. Chapter 6 Phagocytosis and host–pathogen interactions in Dictyostelium with a look at macrophages. Int. Rev. Cell Mol. Biol. 271:253–300
    [Google Scholar]
  17. Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, Stern DL. 2003. Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLOS Biol 1:1e21
    [Google Scholar]
  18. Brelsfoard C, Tsiamis G, Falchetto M, Gomulski LM, Telleria E et al. 2014. Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans morsitans. PLOS Negl. Trop. Dis. 8:4e2728
    [Google Scholar]
  19. Bressan A. 2014. Emergence and evolution of Arsenophonus bacteria as insect-vectored plant pathogens. Infect. Genet. Evol. 22:81–90
    [Google Scholar]
  20. Brown AMV, Howe DK, Wasala SK, Peetz AB, Zasada IA, Denver DR. 2015. Comparative genomics of a plant-parasitic nematode endosymbiont suggest a role in nutritional symbiosis. Genome Biol. Evol. 7:92727–46
    [Google Scholar]
  21. Bublitz DC, Chadwick GL, Magyar JS, Sandoz KM, Brooks DM et al. 2019. Peptidoglycan production by an insect-bacterial mosaic. Cell 179:3703–12.e7
    [Google Scholar]
  22. Buchner P. 1965. Endosymbiosis of Animals with Plant Microorganisms New York: Intersci. Publ.
    [Google Scholar]
  23. Burki F, Roger AJ, Brown MW, Simpson AGB. 2020. The new tree of eukaryotes. Trends Ecol. Evol. 35:143–55
    [Google Scholar]
  24. Büttner D. 2012. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol. . Mol. Biol. Rev. 76:2262–310
    [Google Scholar]
  25. Casadevall A. 2008. Evolution of intracellular pathogens. Annu. Rev. Microbiol. 62:19–33
    [Google Scholar]
  26. Casadevall A. 2012. Amoeba provide insight into the origin of virulence in pathogenic fungi. Adv. Exp. Med. Biol. 710:1–10
    [Google Scholar]
  27. Case EDR, Smith JA, Ficht TA, Samuel JE, de Figueiredo P. 2016. Space: a final frontier for vacuolar pathogens. Traffic 17:5461–74
    [Google Scholar]
  28. Cavalier-Smith T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52:Part 2297–354
    [Google Scholar]
  29. Celli J. 2019. The intracellular life cycle of Brucella spp. Microbiol. Spectr. 7:2 https://doi.org/10.1128/microbiolspec.BAI-0006-2019
    [Crossref] [Google Scholar]
  30. Checroun C, Wehrly TD, Fischer ER, Hayes SF, Celli J 2006. Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. PNAS 103:3914578–83
    [Google Scholar]
  31. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR et al. 2004. Legionella effectors that promote nonlytic release from protozoa. Science 303:56621358–61
    [Google Scholar]
  32. Chen M-C, Cheng Y-M, Sung P-J, Kuo C-E, Fang L-S. 2003. Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem. Biophys. Res. Commun. 308:3586–95
    [Google Scholar]
  33. Cheng LW, Viala JPM, Stuurman N, Wiedemann U, Vale RD, Portnoy DA 2005. Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen. PNAS 102:3813646–51
    [Google Scholar]
  34. Clayton AL, Oakeson KF, Gutin M, Pontes A, Dunn DM et al. 2012. A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect-bacterial symbioses. PLOS Genet 8:11e1002990
    [Google Scholar]
  35. Cornejo E, Schlaermann P, Mukherjee S. 2017. How to rewire the host cell: a home improvement guide for intracellular bacteria. J. Cell Biol. 216:123931–48
    [Google Scholar]
  36. Cossart P, Roy CR, Sansonetti P. 2019. Bacteria and Intracellularity Hoboken, NJ: John Wiley & Sons
    [Google Scholar]
  37. Cossart P, Sansonetti PJ. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:5668242–48
    [Google Scholar]
  38. Dale C, Plague GR, Wang B, Ochman H, Moran NA 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. PNAS 99:1912397–402
    [Google Scholar]
  39. Dance A. 2019. Core Concept: Cells nibble one another via the under-appreciated process of trogocytosis. PNAS 116:3617608–10
    [Google Scholar]
  40. Davy SK, Allemand D, Weis VM. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:2229–61
    [Google Scholar]
  41. De Bary A. 1879. Die Erscheinung Der Symbiose [The Phenomenon of Symbiosis] Strasbourg, Fr: Karl J. Triibner
    [Google Scholar]
  42. de Souza Santos M, Orth K 2020. The role of the type III secretion system in the intracellular lifestyle of enteric pathogens. Bacteria and Intracellularity P Cossart, CR Roy, P Sansonetti 197–214 Hoboken, NJ: John Wiley & Sons
    [Google Scholar]
  43. Deakin WJ, Broughton WJ. 2009. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:4312–20
    [Google Scholar]
  44. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA 2009. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. PNAS 106:229063–68
    [Google Scholar]
  45. Delaye L, Valadez-Cano C, Pérez-Zamorano B. 2016. How really ancient is Paulinella chromatophora?. PLOS Curr 8: ecurrents.tol.e68a099364bb1a1e129a17b4e06b0c6b
    [Google Scholar]
  46. Deretic V, Levine B. 2009. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5:6527–49
    [Google Scholar]
  47. Di Venanzio G, Lazzaro M, Morales ES, Krapf D, Véscovi EG. 2017. A pore-forming toxin enables Serratia a nonlytic egress from host cells. Cell. Microbiol. 19:2e12656
    [Google Scholar]
  48. Djordjevic MA, Gabriel DW, Rolfe BG 1987. Rhizobium—the refined parasite of legumes. Annu. Rev. Phytopathol. 25:145–68
    [Google Scholar]
  49. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:8539–48
    [Google Scholar]
  50. Doherty GJ, McMahon HT. 2009. Mechanisms of endocytosis. Annu. Rev. Biochem. 78:857–902
    [Google Scholar]
  51. Duchêne A-M, Giritch A, Hoffmann B, Cognat V, Lancelin D et al. 2005. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. PNAS 102:4516484–89
    [Google Scholar]
  52. Dunning Hotopp JC, Clark ME, Oliveira DCSG, Foster JM, Fischer P et al. 2007. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:58451753–56
    [Google Scholar]
  53. Embley TM, Martin W. 2006. Eukaryotic evolution, changes and challenges. Nature 440:7084623–30
    [Google Scholar]
  54. Enomoto S, Chari A, Clayton AL, Dale C. 2017. Quorum sensing attenuates virulence in Sodalis praecaptivus. Cell Host Microbe 21:5629–36.e5
    [Google Scholar]
  55. Erken M, Lutz C, McDougald D. 2013. The rise of pathogens: predation as a factor driving the evolution of human pathogens in the environment. Microb. Ecol. 65:4860–68
    [Google Scholar]
  56. Ewald PW. 1987. Transmission modes and evolution of the parasitism-mutualism continuum. Ann. N. Y. Acad. Sci. 503:295–306
    [Google Scholar]
  57. Fairn GD, Grinstein S. 2012. How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33:8397–405
    [Google Scholar]
  58. Ferguson GP, Datta A, Baumgartner J, Roop RM II, Carlson RW, Walker GC 2004. Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. PNAS 101:145012–17
    [Google Scholar]
  59. Fierer N. 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15:10579–90
    [Google Scholar]
  60. Flannagan RS, Jaumouillé V, Grinstein S. 2012. The cell biology of phagocytosis. Annu. Rev. Pathol. 7:61–98
    [Google Scholar]
  61. Flieger A, Frischknecht F, Häcker G, Hornef MW, Pradel G. 2018. Pathways of host cell exit by intracellular pathogens. Microb. Cell Fact. 5:12525–44
    [Google Scholar]
  62. Galán JE, Waksman G. 2018. Protein-injection machines in bacteria. Cell 172:61306–18
    [Google Scholar]
  63. Galperin MY, Wolf YI, Garushyants SK, Vera Alvarez R, Koonin EV 2021. Non-essential ribosomal proteins in bacteria and archaea identified using COGs. J. Bacteriol. 3:JB.00058-21
    [Google Scholar]
  64. Gaudet RG, Bradfield CJ, MacMicking JD. 2016. Evolution of cell-autonomous effector mechanisms in macrophages versus non-immune cells. Microbiol. Spectr. 4:6 https://journals.asm.org/doi/10.1128/microbiolspec.MCHD-0050-2016
    [Google Scholar]
  65. George EE, Husnik F, Tashyreva D, Prokopchuk G, Horák A et al. 2020. Highly reduced genomes of protist endosymbionts show evolutionary convergence. Curr. Biol. 30:5925–33.e3
    [Google Scholar]
  66. Gerstenmaier L, Pilla R, Herrmann L, Herrmann H, Prado M et al. 2015. The autophagic machinery ensures nonlytic transmission of mycobacteria. PNAS 112:7E687–92
    [Google Scholar]
  67. Glazebrook J, Ichige A, Walker GC. 1993. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev 7:81485–97
    [Google Scholar]
  68. Goebel W, Gross R. 2001. Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol 9:6267–73
    [Google Scholar]
  69. Gonçalves WG, Fernandes KM, Silva APA, Gonçalves DG, Fiaz M, Serrão JE. 2020. Ultrastructure of the bacteriocytes in the midgut of the carpenter ant Camponotus rufipes: endosymbiont control by autophagy. Microsc. Microanal 26:61236–44
    [Google Scholar]
  70. Gould SB, Waller RF, McFadden GI. 2008. Plastid evolution. Annu. Rev. Plant Biol. 59:491–517
    [Google Scholar]
  71. Graf JS, Schorn S, Kitzinger K, Ahmerkamp S, Woehle C et al. 2021. Anaerobic endosymbiont generates energy for ciliate host by denitrification. Nature 591:445–50
    [Google Scholar]
  72. Gray MW. 2015. Mosaic nature of the mitochondrial proteome: implications for the origin and evolution of mitochondria. PNAS 112:3310133–38
    [Google Scholar]
  73. Green ER, Mecsas J. 2016. Bacterial secretion systems: an overview. Virulence Mechanisms of Bacterial Pathogens IT Kudva 213–39 Washington, DC: ASM Press
    [Google Scholar]
  74. Hagedorn M, Rohde KH, Russell DG, Soldati T. 2009. Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323:59221729–33
    [Google Scholar]
  75. Hamilton PT, Hodson CN, Curtis CI, Perlman SJ. 2018. Genetics and genomics of an unusual selfish sex ratio distortion in an insect. Curr. Biol. 28:233864–70.e4
    [Google Scholar]
  76. Harb OS, Gao L-Y, Kwaik YA. 2000. From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ. Microbiol 2:3251–65
    [Google Scholar]
  77. Hauben L, Moore ER, Vauterin L, Steenackers M, Mergaert J et al. 1998. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst. Appl. Microbiol. 21:3384–97
    [Google Scholar]
  78. Hentschel U, Steinert M, Hacker J. 2000. Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol 8:5226–31
    [Google Scholar]
  79. Hinde R. 1971. The control of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae. J. Insect Physiol. 17:91791–1800
    [Google Scholar]
  80. Hirano M, Das S, Guo P, Cooper MD. 2011. The evolution of adaptive immunity in vertebrates. Adv. Immunol. 109:125–57
    [Google Scholar]
  81. Hoebe K, Janssen E, Beutler B. 2004. The interface between innate and adaptive immunity. Nat. Immunol. 5:10971–74
    [Google Scholar]
  82. Hoshina R, Imamura N. 2008. Multiple origins of the symbioses in Paramecium bursaria. Protist 159:153–63
    [Google Scholar]
  83. Husnik F, Chrudimský T, Hypša V. 2011. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol 9:87
    [Google Scholar]
  84. Husnik F, Keeling PJ. 2019. The fate of obligate endosymbionts: reduction, integration, or extinction. Curr. Opin. Genet. Dev 58–59:1–8
    [Google Scholar]
  85. Husnik F, McCutcheon JP 2016. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. PNAS 113:37E5416–24
    [Google Scholar]
  86. 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 153:71567–78
    [Google Scholar]
  87. Hybiske K, Stephens RS. 2008. Exit strategies of intracellular pathogens. Nat. Rev. Microbiol. 6:299–110
    [Google Scholar]
  88. Iguchi A, Nagaya Y, Pradel E, Ooka T, Ogura Y et al. 2014. Genome evolution and plasticity of Serratia marcescens, an important multidrug-resistant nosocomial pathogen. Genome Biol. Evol. 6:82096–110
    [Google Scholar]
  89. Ireton K. 2013. Molecular mechanisms of cell-cell spread of intracellular bacterial pathogens. Open Biol 3:7130079
    [Google Scholar]
  90. Jacobovitz MR, Rupp S, Voss PA, Maegele I, Gornik SG, Guse A. 2021. Dinoflagellate symbionts escape vomocytosis by host cell immune suppression. Nat. Microbiol. 6:76982
    [Google Scholar]
  91. Jamwal SV, Mehrotra P, Singh A, Siddiqui Z, Basu A, Rao KVS. 2016. Mycobacterial escape from macrophage phagosomes to the cytoplasm represents an alternate adaptation mechanism. Sci. Rep. 6:23089
    [Google Scholar]
  92. Jenkins BH, Maguire F, Leonard G, Eaton JD, West S et al. 2021. Emergent RNA-RNA interactions can promote stability in a nascent phototrophic endosymbiosis. bioRxiv 439338. https://doi.org/10.1101/2021.04.11.439338
    [Crossref]
  93. Jo E-K, Yuk J-M, Shin D-M, Sasakawa C 2013. Roles of autophagy in elimination of intracellular bacterial pathogens. Front. Immunol. 4:97
    [Google Scholar]
  94. Joly E, Hudrisier D 2003. What is trogocytosis and what is its purpose?. Nat. Immunol. 4:9815
    [Google Scholar]
  95. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:8619–33
    [Google Scholar]
  96. Kambara K, Ardissone S, Kobayashi H, Saad MM, Schumpp O et al. 2009. Rhizobia utilize pathogen-like effector proteins during symbiosis. Mol. Microbiol. 71:192–106
    [Google Scholar]
  97. Karakashian MW, Karakashian SJ. 1973. Intracellular digestion and symbiosis in Paramecium bursaria. Exp. Cell Res. 81:1111–19
    [Google Scholar]
  98. Kazandjian A, Shepherd VA, Rodriguez-Lanetty M, Nordemeier W, Larkum AWD, Quinnell RG. 2008. Isolation of symbiosomes and the symbiosome membrane complex from the zoanthid Zoanthus robustus. Phycologia 47:3294–306
    [Google Scholar]
  99. Keeling PJ. 2010. The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. B 365: 1541 729–48
    [Google Scholar]
  100. Keeling PJ, Burki F. 2019. Progress towards the tree of eukaryotes. Curr. Biol. 29:16R808–17
    [Google Scholar]
  101. Kies L. 1974. Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamfbe mit blau-griinen Endosymbionten (Cyanellen) [Electron microscopic examinations of Paulinella chromatophore Lauterborn, a thecamoeba with blue-green endosymbionts (Glaucophyta)]. Protoplasma 80:69–89
    [Google Scholar]
  102. Kirchberger PC, Schmidt ML, Ochman H. 2020. The ingenuity of bacterial genomes. Annu. Rev. Microbiol. 74:815–34
    [Google Scholar]
  103. Kodama Y, Fujishima M. 2005. Symbiotic Chlorella sp. of the ciliate Paramecium bursaria do not prevent acidification and lysosomal fusion of host digestive vacuoles during infection. Protoplasma 225:3–4191–203
    [Google Scholar]
  104. Kodama Y, Fujishima M. 2010. Secondary symbiosis between Paramecium and Chlorella cells. Int. Rev. Cell Mol. Biol. 279:33–77
    [Google Scholar]
  105. Koga R, Meng X-Y, Tsuchida T, Fukatsu T. 2008. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. PNAS 109:20E1230–37
    [Google Scholar]
  106. Kořený L, Oborník M, Lukeš J. 2013. Make it, take it, or leave it: heme metabolism of parasites. PLOS Pathog 9:1e1003088
    [Google Scholar]
  107. Koskella B. 2020. The phyllosphere. Curr. Biol. 30:19PR1143–46
    [Google Scholar]
  108. Koumandou VL, Wickstead B, Ginger ML, van der Giezen M, Dacks JB, Field MC. 2013. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48:4373–96
    [Google Scholar]
  109. Kozek WJ. 1977. Transovarially-transmitted intracellular microorganisms in adult and larval stages of Brugia malayi. J. Parasitol. 63:6992–1000
    [Google Scholar]
  110. Ku C, Nelson-Sathi S, Roettger M, Garg S, Hazkani-Covo E, Martin WF. 2015. Endosymbiotic gene transfer from prokaryotic pangenomes: inherited chimerism in eukaryotes. PNAS 112:3310139–46
    [Google Scholar]
  111. Kupper M, Stigloher C, Feldhaar H, Gross R. 2016. Distribution of the obligate endosymbiont Blochmannia floridanus and expression analysis of putative immune genes in ovaries of the carpenter ant Camponotus floridanus. Arthropod Struct. Dev. 45:5475–87
    [Google Scholar]
  112. Lamelas A, Gosalbes MJ, Manzano-Marín A, Peretó J, Moya A, Latorre A. 2011. Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLOS Genet 7:11e1002357
    [Google Scholar]
  113. Lancaster CE, Ho CY, Hipolito VEB, Botelho RJ, Terebiznik MR. 2019. Phagocytosis: what's on the menu?. Biochem. Cell Biol. 97:12129
    [Google Scholar]
  114. Landmann F. 2019. The Wolbachia endosymbionts. Microbiol. Spectr 7:2 https://doi.org/10.1128/9781683670261.ch10
    [Crossref] [Google Scholar]
  115. Landmann F, Bain O, Martin C, Uni S, Taylor MJ, Sullivan W. 2012. Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biol. Open 1:6536–47
    [Google Scholar]
  116. Lane N, Martin WF. 2015. Eukaryotes really are special, and mitochondria are why. PNAS 112:35E4823
    [Google Scholar]
  117. Lawen A. 2003. Apoptosis—an introduction. Bioessays 25:9888–96
    [Google Scholar]
  118. Lawrence JG. 2005. Common themes in the genome strategies of pathogens. Curr. Opin. Genet. Dev. 15:6584–88
    [Google Scholar]
  119. Leclercq S, Cloeckaert A, Zygmunt MS. 2019. Taxonomic organization of the family Brucellaceae based on a phylogenomic approach. Front. Microbiol. 10:3083
    [Google Scholar]
  120. Leclercq S, Thézé J, Chebbi MA, Giraud I, Moumen B et al. 2016. Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. PNAS 113:5215036–41
    [Google Scholar]
  121. Loh J, Pierson EA, Pierson LS III, Stacey G, Chatterjee A. 2002. Quorum sensing in plant-associated bacteria. Curr. Opin. Plant Biol. 5:4285–90
    [Google Scholar]
  122. Lowe CD, Minter EJ, Cameron DD, Brockhurst MA. 2016. Shining a light on exploitative host control in a photosynthetic endosymbiosis. Curr. Biol. 26:2207–11
    [Google Scholar]
  123. Luan J-B, Chen W, 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. 7:92635–47
    [Google Scholar]
  124. Ma H, Croudace JE, Lammas DA, May RC 2006. Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 16:212156–60
    [Google Scholar]
  125. Maire J, Parisot N, Galvao Ferrarini M, Vallier A, Gillet B et al. 2020. Spatial and morphological reorganization of endosymbiosis during metamorphosis accommodates adult metabolic requirements in a weevil. PNAS 117:3219347–58
    [Google Scholar]
  126. Manzano-Marín A, Latorre A. 2014. Settling down: the genome of Serratia symbiotica from the aphid Cinara tujafilina zooms in on the process of accommodation to a cooperative intracellular life. Genome Biol. Evol. 6:71683–98
    [Google Scholar]
  127. Manzano-Marín A, Latorre A. 2016. Snapshots of a shrinking partner: genome reduction in Serratia symbiotica. Sci. Rep. 6:32590
    [Google Scholar]
  128. Marin B, Nowack ECM, Melkonian M. 2005. A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:4425–32
    [Google Scholar]
  129. Martinson VG, Gawryluk RMR, Gowen BE, Curtis CI, Jaenike J, Perlman SJ 2020. Multiple origins of obligate nematode and insect symbionts by a clade of bacteria closely related to plant pathogens. PNAS 117:5031979–86
    [Google Scholar]
  130. Masson F, Moné Y, Vigneron A, Vallier A, Parisot N et al. 2015. Weevil endosymbiont dynamics is associated with a clamping of immunity. BMC Genom 16:819
    [Google Scholar]
  131. Matz C, Kjelleberg S. 2005. Off the hook – how bacteria survive protozoan grazing. Trends Microbiol 13:7302–7
    [Google Scholar]
  132. McCutcheon JP. 2010. The bacterial essence of tiny symbiont genomes. Curr. Opin. Microbiol. 13:173–78
    [Google Scholar]
  133. McCutcheon JP, Boyd BM, Dale C. 2019. The life of an insect endosymbiont from the cradle to the grave. Curr. Biol. 29:11R485–95
    [Google Scholar]
  134. McCutcheon JP, Moran NA. 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:113–26
    [Google Scholar]
  135. McFadden GI. 2001. Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37:6951–59
    [Google Scholar]
  136. McLaughlin RN Jr., Malik HS. 2017. Genetic conflicts: the usual suspects and beyond. J. Exp. Biol. 220:Part 16–17
    [Google Scholar]
  137. Mills DB. 2020. The origin of phagocytosis in Earth history. Interface Focus 10:420200019
    [Google Scholar]
  138. Mohamed AR, Cumbo V, Harii S, Shinzato C, Chan CX et al. 2016. The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome. Mol. Ecol. 25:133127–41
    [Google Scholar]
  139. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y 2005. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71:120–28
    [Google Scholar]
  140. Monack DM, Mueller A, Falkow S. 2004. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat. Rev. Microbiol. 2:9747–65
    [Google Scholar]
  141. Moran NA. 1992. The evolution of aphid life cycles. Annu. Rev. Entomol. 37:321–48
    [Google Scholar]
  142. Moran NA. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:5583–86
    [Google Scholar]
  143. Moran NA, Bennett GM. 2014. The tiniest tiny genomes. Annu. Rev. Microbiol. 68:195–215
    [Google Scholar]
  144. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165–90
    [Google Scholar]
  145. Moran NA, Plague GR, Sandström JP, Wilcox JL 2003. A genomic perspective on nutrient provisioning by bacterial symbionts of insects. PNAS 100:Suppl. 214543–48
    [Google Scholar]
  146. Moran NA, Russell JA, Koga R, Fukatsu T. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71:63302–10
    [Google Scholar]
  147. Morisaki JH, Heuser JE, Sibley LD. 1995. Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108:Part 62457–64
    [Google Scholar]
  148. Munoz MM, Spencer N, Enomoto S, Dale C, Rio RVM. 2020. Quorum sensing sets the stage for the establishment and vertical transmission of Sodalis praecaptivus in tsetse flies. PLOS Genet 16:8e1008992
    [Google Scholar]
  149. Muscatine L, Porter JW. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:7454–60
    [Google Scholar]
  150. Nakabachi A, Ishida K, Hongoh Y, Ohkuma M, Miyagishima S-Y. 2014. Aphid gene of bacterial origin encodes a protein transported to an obligate endosymbiont. Curr. Biol. 24:14R640–41
    [Google Scholar]
  151. Nardon P, Charles H, Delobel B, Lefevre C, Heddi A 2003. Symbiosis in the dryophthoridae weevils (Coleoptera, Curculionoidea): morphological variability of symbiotic intracellular bacteria. Symbiosis 34:323151
    [Google Scholar]
  152. Needham BD, Trent MS. 2013. Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat. Rev. Microbiol. 11:7467–81
    [Google Scholar]
  153. Nikoh N, McCutcheon JP, Kudo T, Miyagishima S-Y, Moran NA, Nakabachi A. 2010. Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLOS Genet 6:2e1000827
    [Google Scholar]
  154. Nikoh N, Nakabachi A. 2009. Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 7:12
    [Google Scholar]
  155. Nishikori K, Morioka K, Kubo T, Morioka M. 2009. Age- and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis. J. Insect Physiol. 55:4351–57
    [Google Scholar]
  156. Nováková E, Hypsa V, Moran NA. 2009. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9:143
    [Google Scholar]
  157. Nowack ECM, Grossman AR 2012. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. PNAS 109:145340–45
    [Google Scholar]
  158. Nowack ECM, Melkonian M. 2010. Endosymbiotic associations within protists. Philos. Trans. R. Soc. B 365: 1541.699–712
    [Google Scholar]
  159. Nowack ECM, Melkonian M, Glöckner G. 2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18:6410–18
    [Google Scholar]
  160. Nowack ECM, Price DC, Bhattacharya D, Singer A, Melkonian M, Grossman AR 2016. Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. PNAS 113:4312214–19
    [Google Scholar]
  161. Nowack ECM, Weber APM. 2018. Genomics-informed insights into endosymbiotic organelle evolution in photosynthetic eukaryotes. Annu. Rev. Plant Biol. 69:51–84
    [Google Scholar]
  162. Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC et al. 2014. Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol. Evol. 6:176–93
    [Google Scholar]
  163. Ochman H, Davalos LM. 2006. The nature and dynamics of bacterial genomes. Science 311:57681730–33
    [Google Scholar]
  164. Ohl ME, Miller SI. 2001. Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52:259–74
    [Google Scholar]
  165. Oke V, Long SR. 1999. Bacteroid formation in the Rhizobium-legume symbiosis. Curr. Opin. Microbiol. 2:6641–46
    [Google Scholar]
  166. Oldroyd GED, Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45:119–44
    [Google Scholar]
  167. Omotade TO, Roy CR. 2019. Manipulation of host cell organelles by intracellular pathogens. Microbiol. Spectr 7:2 https://doi.org/10.1128/microbiolspec.BAI-0022-2019
    [Crossref] [Google Scholar]
  168. Oulhen N, Schulz BJ, Carrier TJ. 2016. English translation of Heinrich Anton de Bary's 1878 speech, ‘Die Erscheinung der Symbiose’ (‘De la symbiose’) [The Phenomenon of Symbiosis]. Symbiosis 69:131–39
    [Google Scholar]
  169. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB et al. 2008. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:1112–23
    [Google Scholar]
  170. Pawlowska TE, Gaspar ML, Lastovetsky OA, Mondo SJ, Real-Ramirez I et al. 2018. Biology of fungi and their bacterial endosymbionts. Annu. Rev. Phytopathol. 56:289–309
    [Google Scholar]
  171. Perreau J, Patel DJ, Anderson H, Maeda GP, Elston KM et al. 2021. Vertical transmission at the pathogen-symbiont interface: Serratia symbiotica and aphids. mBio 12:2 https://doi.org/10.1128/mBio.00359-21
    [Crossref] [Google Scholar]
  172. Petersen LM, Tisa LS. 2013. Friend or foe? A review of the mechanisms that drive Serratia towards diverse lifestyles. Can. J. Microbiol. 59:9627–40
    [Google Scholar]
  173. Pfanner N, Meijer M. 1997. Mitochondrial biogenesis: the Tom and Tim machine. Curr. Biol. 7:2R100–3
    [Google Scholar]
  174. Philips JA, Rubin EJ, Perrimon N. 2005. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309:57381251–53
    [Google Scholar]
  175. Pieters J. 2008. Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3:6399–407
    [Google Scholar]
  176. Pons I, Renoz F, Noël C, Hance T. 2019a. Circulation of the cultivable symbiont Serratia symbiotica in aphids is mediated by plants. Front. Microbiol. 10:764
    [Google Scholar]
  177. Pons I, Renoz F, Noël C, Hance T. 2019b. New insights into the nature of symbiotic associations in aphids: infection process, biological effects, and transmission mode of cultivable Serratia symbiotica bacteria. Appl. Environ. Microbiol. 85:10e02445
    [Google Scholar]
  178. Poole AM, Gribaldo S. 2014. Eukaryotic origins: how and when was the mitochondrion acquired?. Cold Spring Harb. Perspect. Biol. 6:12a015990
    [Google Scholar]
  179. Prashar A, Terebiznik MR. 2015. Legionella pneumophila: homeward bound away from the phagosome. Curr. Opin. Microbiol. 23:86–93
    [Google Scholar]
  180. Qiu H, Price DC, Weber APM, Facchinelli F, Yoon HS, Bhattacharya D. 2013. Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci 18:12680–87
    [Google Scholar]
  181. Randow F, MacMicking JD, James LC. 2013. Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340:6133701–6
    [Google Scholar]
  182. Ray K, Marteyn B, Sansonetti PJ, Tang CM. 2009. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat. Rev. Microbiol. 7:5333–40
    [Google Scholar]
  183. Renoz F, Pons I, Vanderpoorten A, Bataille G, Noël C et al. 2019. Evidence for gut-associated Serratia symbiotica in wild aphids and ants provides new perspectives on the evolution of bacterial mutualism in insects. Microb. Ecol. 78:1159–69
    [Google Scholar]
  184. Reumann S, Inoue K, Keegstra K. 2005. Evolution of the general protein import pathway of plastids (review). Mol. Membr. Biol. 22:1–273–86
    [Google Scholar]
  185. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. 2005. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:5735–49
    [Google Scholar]
  186. Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G et al. 2005. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15:141325–30
    [Google Scholar]
  187. Roger AJ, Muñoz-Gómez SA, Kamikawa R 2017. The origin and diversification of mitochondria. Curr. Biol. 27:21R1177–92
    [Google Scholar]
  188. Rother M, Teixeira da Costa AR, Zietlow R, Meyer TF, Rudel T 2019. Modulation of host cell metabolism by Chlamydia trachomatis. Microbiol. Spectr. 7:3 https://doi.org/10.1128/microbiolspec.BAI-0012-2019
    [Crossref] [Google Scholar]
  189. Ruby T, McLaughlin L, Gopinath S, Monack D. 2012. Salmonella’s long-term relationship with its host. FEMS Microbiol. Rev. 36:3600–615
    [Google Scholar]
  190. Russell DG. 2001. Mycobacterium tuberculosis: here today, and here tomorrow. Nat. Rev. Mol. Cell Biol. 2:8569–77
    [Google Scholar]
  191. Russell DG. 2007. Phagocytosis. eLS https://doi.org/10.1002/9780470015902.a0000488.pub2
    [Crossref] [Google Scholar]
  192. Russell SL, Chappell L, Sullivan W. 2019. A symbiont's guide to the germline. Curr. Top. Dev. Biol. 135:315–51
    [Google Scholar]
  193. Sachs JL, Essenberg CJ, Turcotte MM. 2011. New paradigms for the evolution of beneficial infections. Trends Ecol. Evol. 26:4202–9
    [Google Scholar]
  194. Sachs JL, Quides KW, Wendlandt CE. 2018. Legumes versus rhizobia: a model for ongoing conflict in symbiosis. New Phytol 219:41199–206
    [Google Scholar]
  195. Sapp J. 1994. Evolution by Association: A History of Symbiosis Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  196. Sato N, Yoshitomi T, Mori-Moriyama N. 2020. Characterization and biosynthesis of lipids in Paulinella micropora MYN1: evidence for efficient integration of chromatophores into cellular lipid metabolism. Plant Cell Physiol 61:5869–81
    [Google Scholar]
  197. Schmidt O, Pfanner N, Meisinger C. 2010. Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11:9655–67
    [Google Scholar]
  198. Schröder D, Deppisch H, Obermayer M, Krohne G, Stackebrandt E et al. 1996. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol. Microbiol. 21:3479–89
    [Google Scholar]
  199. Seoane PI, May RC. 2020. Vomocytosis: what we know so far. Cell. Microbiol. 22:2e13145
    [Google Scholar]
  200. Serbus LR, Sullivan W. 2007. A cellular basis for Wolbachia recruitment to the host germline. PLOS Pathog 3:12e190
    [Google Scholar]
  201. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:680081–86
    [Google Scholar]
  202. Siegel RW. 1960. Hereditary endosymbiosis in Paramecium bursaria. Exp. Cell Res. 19:239–52
    [Google Scholar]
  203. Simonet P, Gaget K, Balmand S, Ribeiro Lopes M, Parisot N et al. 2018. Bacteriocyte cell death in the pea aphid/Buchnera symbiotic system. PNAS 115:8E1819–28
    [Google Scholar]
  204. Simpson AGB, Eglit Y. 2016. Protist diversification. Encycl. Evol. Biol. 3:344–60
    [Google Scholar]
  205. Singer A, Poschmann G, Mühlich C, Valadez-Cano C, Hänsch S et al. 2017. Massive protein import into the early-evolutionary-stage photosynthetic organelle of the amoeba Paulinella chromatophora. Curr. Biol. 27:182763–73.e5
    [Google Scholar]
  206. 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. 31:4857–71
    [Google Scholar]
  207. Smith DR, Keeling PJ. 2015. Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. PNAS 112:3310177–84
    [Google Scholar]
  208. Sommer F, Bäckhed F. 2013. The gut microbiota—masters of host development and physiology. Nat. Rev. 11:227–38
    [Google Scholar]
  209. Soo RM, Hemp J, Parks DH, Fischer WW, Hugenholtz P. 2017. On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 355:63321436–40
    [Google Scholar]
  210. Soto MJ, Sanjuán J, Olivares J. 2006. Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiology 152:Part 113167–74
    [Google Scholar]
  211. Stairs CW, Dharamshi JE, Tamarit D, Eme L, Jørgensen SL et al. 2020. Chlamydial contribution to anaerobic metabolism during eukaryotic evolution. Sci. Adv. 6:35eabb7258
    [Google Scholar]
  212. Starr T, Child R, Wehrly TD, Hansen B, Hwang S et al. 2012. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 11:133–45
    [Google Scholar]
  213. Steele S, Radlinski L, Taft-Benz S, Brunton J, Kawula TH 2016. Trogocytosis-associated cell to cell spread of intracellular bacterial pathogens. eLife 5:e10625
    [Google Scholar]
  214. Steele-Mortimer O. 2008. The Salmonella-containing vacuole—moving with the times. Curr. Opin. Microbiol. 11:138–45
    [Google Scholar]
  215. Steenbergen JN, Shuman HA, Casadevall A 2001. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. PNAS 98:2615245–50
    [Google Scholar]
  216. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:8513–25
    [Google Scholar]
  217. Stoll S, Feldhaar H, Fraunholz MJ, Gross R. 2010. Bacteriocyte dynamics during development of a holometabolous insect, the carpenter ant Camponotus floridanus. BMC Microbiol 10:308
    [Google Scholar]
  218. Swanson MS, Hammer BK. 2000. Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54:567–613
    [Google Scholar]
  219. Szklarzewicz T, Michalik A 2017. Transovarial transmission of symbionts in insects. Results and Problems in Cell Differentiation, Vol. 63 M Kloc 43–67 Berlin/Heidelberg: Springer
    [Google Scholar]
  220. Tam JCH, Jacques DA. 2014. Intracellular immunity: finding the enemy within—how cells recognize and respond to intracellular pathogens. J. Leukoc. Biol. 96:2233–44
    [Google Scholar]
  221. Toju H, Tanabe AS, Notsu Y, Sota T, Fukatsu T. 2013. Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J 7:71378–90
    [Google Scholar]
  222. Unterman BM, Baumann P, McLean DL. 1989. Pea aphid symbiont relationships established by analysis of 16S rRNAs. J. Bacteriol. 171:62970–74
    [Google Scholar]
  223. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M et al. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:71287–98
    [Google Scholar]
  224. Veiga E, Guttman JA, Bonazzi M, Boucrot E, Toledo-Arana A et al. 2007. Invasive and adherent bacterial pathogens co-opt host clathrin for infection. Cell Host Microbe 2:5340–51
    [Google Scholar]
  225. Vigneron A, Masson F, Vallier A, Balmand S, Rey M et al. 2014. Insects recycle endosymbionts when the benefit is over. Curr. Biol. 24:192267–73
    [Google Scholar]
  226. Walterson AM, Stavrinides J. 2015. Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol. Rev. 39:6968–84
    [Google Scholar]
  227. Watkins RA, Andrews A, Wynn C, Barisch C, King JS, Johnston SA. 2018. Cryptococcus neoformans escape from Dictyostelium amoeba by both WASH-mediated constitutive exocytosis and vomocytosis. Front. Cell. Infect. Microbiol. 8:108
    [Google Scholar]
  228. Werren JH, Baldo L, Clark ME. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6:10741–51
    [Google Scholar]
  229. Whelan J. 1999. Plant mitochondrial protein import: mechanisms and control. Funct. Plant Biol. 26:8725–32
    [Google Scholar]
  230. White PM, Pietri JE, Debec A, Russell S, Patel B, Sullivan W 2017. Mechanisms of horizontal cell-to-cell transfer of Wolbachia spp. in Drosophila melanogaster. Appl. Environ. Microbiol. 83:7e03425
    [Google Scholar]
  231. Wilkinson TL, Fukatsu T, Ishikawa H. 2003. Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arthropod Struct. Dev. 32:2–3241–45
    [Google Scholar]
  232. Williams KP, Gillespie JJ, Sobral BWS, Nordberg EK, Snyder EE et al. 2010. Phylogeny of gammaproteobacteria. J. Bacteriol. 192:92305–14
    [Google Scholar]
  233. Wilson ACC 2020. Regulation of an insect symbiosis. Advances in Insect Physiology, Vol. 58 KM Oliver, JA Russell 207–31 London: Acad. Press
    [Google Scholar]
  234. Young D, Hussell T, Dougan G. 2002. Chronic bacterial infections: living with unwanted guests. Nat. Immunol. 3:111026–32
    [Google Scholar]
  235. Young JP, Johnston AW. 1989. The evolution of specificity in the legume-rhizobium symbiosis. Trends Ecol. Evol. 4:11341–49
    [Google Scholar]
  236. Zahran HH. 1999. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. . Mol. Biol. Rev. 63:4968–89
    [Google Scholar]
  237. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L et al. 2017. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:7637353–58
    [Google Scholar]
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