1887

Abstract

Not long ago, protists were considered one of four eukaryote kingdoms, but recent gene-based phylogenies show that they contribute to all nine eukaryote subdomains. The former kingdoms of animals, plants and fungi are now relegated to lower ranks within subdomains. Most unicellular protists respond to adverse conditions by differentiating into dormant walled cysts. As cysts, they survive long periods of starvation, drought and other environmental threats, only to re-emerge when conditions improve. For protists pathogens, the resilience of their cysts can prevent successful treatment or eradication of the disease. In this context, effort has been directed towards understanding the molecular mechanisms that control encystation. We here firstly summarize the prevalence of encystation across protists and next focus on Amoebozoa, where most of the health-related issues occur. We review current data on processes and genes involved in encystation of the obligate parasite Entamoeba histolytica and the opportunistic pathogen Acanthamoeba. We show how the cAMP-mediated signalling pathway that controls spore and stalk cell encapsulation in Dictyostelium fruiting bodies could be retraced to a stress-induced pathway controlling encystation in solitary Amoebozoa. We highlight the conservation and prevalence of cAMP signalling genes in Amoebozoan genomes and the suprisingly large and varied repertoire of proteins for sensing and processing environmental signals in individual species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000653
2018-04-05
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/5/727.html?itemId=/content/journal/micro/10.1099/mic.0.000653&mimeType=html&fmt=ahah

References

  1. Shmakova L, Bondarenko N, Smirnov A. Viable species of Flamella (Amoebozoa: Variosea) isolated from ancient Arctic permafrost sediments. Protist 2016; 167: 13– 30 [CrossRef]
    [Google Scholar]
  2. Lloyd D, Turner NA, Khunkitti W, Hann AC, Furr JR et al. Encystation in Acanthamoeba castellanii: development of biocide resistance. J Eukaryot Microbiol 2001; 48: 11– 16 [CrossRef]
    [Google Scholar]
  3. Aksozek A, McClellan K, Howard K, Niederkorn JY, Alizadeh H. Resistance of Acanthamoeba castellanii cysts to physical, chemical, and radiological conditions. J Parasitol 2002; 88: 621– 623 [CrossRef]
    [Google Scholar]
  4. Hurt M, Proy V, Niederkorn JY, Alizadeh H. The interaction of Acanthamoeba castellanii cysts with macrophages and neutrophils. J Parasitol 2003; 89: 565– 572 [CrossRef]
    [Google Scholar]
  5. Abd H, Saeed A, Weintraub A, Nair GB, Sandstrom G. Vibrio cholerae O1 strains are facultative intracellular bacteria, able to survive and multiply symbiotically inside the aquatic free-living amoeba Acanthamoeba castellanii. FEMS Microbiol Ecol 2007; 60: 33– 39 [CrossRef]
    [Google Scholar]
  6. Wheat WH, Casali AL, Thomas V, Spencer JS, Lahiri R et al. Long-term survival and virulence of Mycobacterium leprae in amoebal cysts. PLoS Negl Trop Dis 2014; 8: e3405 [CrossRef]
    [Google Scholar]
  7. Storey MV, Winiecka-Krusnell J, Ashbolt NJ, Stenström TA. The efficacy of heat and chlorine treatment against thermotolerant Acanthamoebae and Legionellae. Scand J Infect Dis 2004; 36: 656– 662 [CrossRef]
    [Google Scholar]
  8. de Souza TK, Soares SS, Benitez LB, Rott MB. Interaction between methicillin-resistant Staphylococcus aureus (MRSA) and Acanthamoeba polyphaga. Curr Microbiol 2017; 74: 541– 549 [CrossRef]
    [Google Scholar]
  9. Scheikl U, Sommer R, Kirschner A, Rameder A, Schrammel B et al. Free-living amoebae (FLA) co-occurring with legionellae in industrial waters. Eur J Protistol 2014; 50: 422– 429 [CrossRef]
    [Google Scholar]
  10. Margulis L. Biodiversity: molecular biological domains, symbiosis and kingdom origins. Biosystems 1992; 27: 39– 51 [CrossRef]
    [Google Scholar]
  11. He D, Fiz-Palacios O, Fu C-J, Fehling J, Tsai C-C et al. An alternative root for the eukaryote tree of life. Current Biology 2014; 24: 465– 470 [CrossRef]
    [Google Scholar]
  12. Kang S, Tice AK, Spiegel FW, Silberman JD, Pánek T et al. Between a pod and a hard test: the deep evolution of amoebae. Mol Biol Evol 2017; 34: 2258– 2270 [CrossRef]
    [Google Scholar]
  13. O'Kelly CJ. Ultrastructure of trophozoites, zoospores and cysts of Reclinomonas americana Flavin & Nerad, 1993 (Protista incertae sedis: Histionidae). Eur J Protistol 1997; 33: 337– 348 [CrossRef]
    [Google Scholar]
  14. Aguilar-Díaz H, Carrero JC, Argüello-García R, Laclette JP, Morales-Montor J. Cyst and encystment in protozoan parasites: optimal targets for new life-cycle interrupting strategies?. Trends Parasitol 2011; 27: 450– 458 [CrossRef]
    [Google Scholar]
  15. Hindák F, Wolowski K, Hindáková A. Cysts and their formation in some neustonic Euglena species. Annals of Limnology 2000; 36: 83– 93 [CrossRef]
    [Google Scholar]
  16. Sekimoto H. Sexual reproduction and sex determination in green algae. J Plant Res 2017; 130: 423– 431 [CrossRef]
    [Google Scholar]
  17. Vandenhoff J, Burton HR, Vesk M. An encystment stage, bearing a new scale type, of the antarctic prasinophyte Pyramimonas-gelidicola and its paleolimnological and taxonomic significance. J Phycol 1989; 25: 446– 454 [Crossref]
    [Google Scholar]
  18. Ellegaard M, Moestrup Ø, Joest Andersen T, Lundholm N. Long-term survival of haptophyte and prasinophyte resting stages in marine sediment. Eur J Phycol 2016; 51: 328– 337 [CrossRef]
    [Google Scholar]
  19. Ellegaard M, Ribeiro S. The long-term persistence of phytoplankton resting stages in aquatic ‘seed banks’. Biological Reviews 2018; 93: 166– 183 [CrossRef]
    [Google Scholar]
  20. Lewis J, Harris ASD, Jones KJ, Edmonds RL. Long-term survival of marine planktonic diatoms and dinoflagellates in stored sediment samples. J Plankton Res 1999; 21: 343– 354 [CrossRef]
    [Google Scholar]
  21. Holen DA. Chrysophyte stomatocyst production in laboratory culture and descriptions of seven cyst morphotypes. Phycologia 2014; 53: 426– 432 [CrossRef]
    [Google Scholar]
  22. Judelson HS, Blanco FA. The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 2005; 3: 47– 58 [CrossRef]
    [Google Scholar]
  23. Dumack K, Baumann C, Bonkowski M. A bowl with marbles: revision of the thecate amoeba genus Lecythium (Chlamydophryidae, Tectofilosida, Cercozoa, Rhizaria) including a description of four new species and an identification key. Protist 2016; 167: 440– 459 [CrossRef]
    [Google Scholar]
  24. Decelle J, Martin P, Paborstava K, Pond DW, Tarling G et al. Diversity, ecology and biogeochemistry of cyst-forming Acantharia (Radiolaria) in the oceans. PLoS One 2013; 8: 13 [CrossRef]
    [Google Scholar]
  25. Verni F, Rosati G. Resting cysts: a survival strategy in Protozoa Ciliophora. Ital J Zool 2011; 78: 134– 145 [CrossRef]
    [Google Scholar]
  26. Bravo I, Figueroa R. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2014; 2: 11– 32 [CrossRef]
    [Google Scholar]
  27. Sullivan WJ, Jeffers V. Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol Rev 2012; 36: 717– 733 [CrossRef]
    [Google Scholar]
  28. Dubey JP, Lindsay DS, Speer CA. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev 1998; 11: 267– 299 [PubMed]
    [Google Scholar]
  29. Brown MW, Spiegel FW, Silberman JD. Phylogeny of the "forgotten" cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Mol Biol Evol 2009; 26: 2699– 2709 [CrossRef]
    [Google Scholar]
  30. Worley AC, Raper KB, Hohl M. Fonticula alba: a new cellular slime mold (Acrasiomycetes). Mycologia 1979; 71: 746– 760 [CrossRef]
    [Google Scholar]
  31. Leadbeater BSC, Karpov SA. Cyst formation in a freshwater strain of the choanoflagellate desmarella moniliformis kent. J Eukaryot Microbiol 2000; 47: 433– 439 [CrossRef]
    [Google Scholar]
  32. Sebé-Pedrós A, Irimia M, del Campo J, Parra-Acero H, Russ C et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2013; 2: e01287 [CrossRef]
    [Google Scholar]
  33. Cavalier-Smith T, Chao EE-Y, Oates B. Molecular phylogeny of amoebozoa and the evolutionary significance of the unikont Phalansterium. Eur J Protistol 2004; 40: 21– 48 [CrossRef]
    [Google Scholar]
  34. Shadwick LL, Spiegel FW, Shadwick JDL, Brown MW, Silberman JD. Eumycetozoa = amoebozoa?: ssurdna phylogeny of protosteloid slime molds and its significance for the amoebozoan supergroup. PLoS One 2009; 4: e6754 [CrossRef]
    [Google Scholar]
  35. Cavalier-Smith T, Chao EE, Lewis R. 187-gene phylogeny of protozoan phylum Amoebozoa reveals a new class (Cutosea) of deep-branching, ultrastructurally unique, enveloped marine Lobosa and clarifies amoeba evolution. Mol Phylogenet Evol 2016; 99: 275– 296 [CrossRef]
    [Google Scholar]
  36. Lahr DJG, Parfrey LW, Mitchell EAD, Katz LA, Lara E. The chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms. Proc Biol Sci 2011; 278: 2081– 2090 [CrossRef]
    [Google Scholar]
  37. Spiegel FW. Commentary on the chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms. Proc Biol Sci 2011; 278: 2096– 2097 [CrossRef]
    [Google Scholar]
  38. Hillmann F, Forbes G, Novohradská S, Ferling I, Riege K et al. Multiple roots of fruiting body formation in amoebozoa. Genome Biol Evol 2018; 10: 591– 606 [CrossRef]
    [Google Scholar]
  39. Hellebø A, Stene A, Aspehaug V. PCR survey for Paramoeba perurans in fauna, environmental samples and fish associated with marine farming sites for Atlantic salmon (Salmo salar L.). J Fish Dis 2017; 40: 661– 670 [CrossRef]
    [Google Scholar]
  40. Feehan CJ, Johnson-Mackinnon J, Scheibling RE, Lauzon-Guay JS, Simpson AGB. Validating the identity of Paramoeba invadens, the causative agent of recurrent mass mortality of sea urchins in Nova Scotia, Canada. Dis Aquat Organ 2013; 103: 209– 227 [CrossRef]
    [Google Scholar]
  41. WHO Amoebiasis. Releve Epidemiologique Hebdomadairevol. 72 1997; pp. 97– 99
    [Google Scholar]
  42. Vazquezdelara-Cisneros LG, Arroyo-Begovich A. Induction of encystation of Entamoeba invadens by removal of glucose from the culture medium. J Parasitol 1984; 70: 629– 633 [CrossRef]
    [Google Scholar]
  43. Coppi A, Merali S, Eichinger D. The enteric parasite Entamoeba uses an autocrine catecholamine system during differentiation into the infectious cyst stage. J Biol Chem 2002; 277: 8083– 8090 [CrossRef] [PubMed]
    [Google Scholar]
  44. Mi-Ichi F, Miyamoto T, Takao S, Jeelani G, Hashimoto T et al. Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis. Proc Natl Acad Sci USA 2015; 112: E2884 E2890 [CrossRef]
    [Google Scholar]
  45. Loftus B, Anderson I, Davies R, Alsmark UCM, Samuelson J et al. The genome of the protist parasite Entamoeba histolytica. Nature 2005; 433: 865– 868 [CrossRef]
    [Google Scholar]
  46. Wang Z, Samuelson J, Clark CG, Eichinger D, Paul J et al. Gene discovery in the Entamoeba invadens genome. Mol Biochem Parasitol 2003; 129: 23– 31 [CrossRef]
    [Google Scholar]
  47. Arroyo-Begovich A, Cárabez-Trejo A, Ruíz-Herrera J, Carabez-Trejo A, Ruiz-Herrera J. Identification of the structural component in the cyst wall of Entamoeba invadens. J Parasitol 1980; 66: 735– 741 [CrossRef]
    [Google Scholar]
  48. Eichinger D. A role for a galactose lectin and its ligands during encystment of Entamoeba. J Eukaryot Microbiol 2001; 48: 17– 21 [CrossRef]
    [Google Scholar]
  49. Samuelson J, Robbins P. A simple fibril and lectin model for cyst walls of Entamoeba and perhaps Giardia. Trends Parasitol 2011; 27: 17– 22 [CrossRef]
    [Google Scholar]
  50. Singh M, Sharma S, Bhattacharya A, Tatu U. Heat shock protein 90 regulates encystation in Entamoeba. Front Microbiol 2015; 6: 1125 [CrossRef]
    [Google Scholar]
  51. Sharma M, Hirata K, Herdman S, Reed S. Entamoeba invadens:characterization of cysteine proteinases. Exp Parasitol 1996; 84: 84– 91 [CrossRef]
    [Google Scholar]
  52. de Meester F, Shaw E, Scholze H, Stolarsky T, Mirelman D. Specific labeling of cysteine proteinases in pathogenic and nonpathogenic Entamoeba histolytica. Infect Immun 1990; 58: 1396– 1401 [PubMed]
    [Google Scholar]
  53. Gonzalez J, Bai G, Frevert U, Corey EJ, Eichinger D. Proteasome-dependent cyst formation and stage-specific ubiquitin mRNA accumulation in Entamoeba invadens. Eur J Biochem 1999; 264: 897– 904 [CrossRef]
    [Google Scholar]
  54. Makioka A, Kumagai M, Ohtomo H, Kobayashi S, Takeuchi T. Effect of proteasome inhibitors on the growth, encystation, and excystation of Entamoeba histolytica and Entamoeba invadens. Parasitol Res 2002; 88: 454– 459 [CrossRef]
    [Google Scholar]
  55. Mi-Ichi F, Yoshida H, Hamano S. Entamoeba encystation: new targets to prevent the transmission of amebiasis. PLoS Pathog 2016; 12: e1005845 [CrossRef]
    [Google Scholar]
  56. Hamann L, Nickel R, Tannich E. Transfection and continuous expression of heterologous genes in the protozoan parasite Entamoeba histolytica. Proc Natl Acad Sci USA 1995; 92: 8975– 8979 [CrossRef]
    [Google Scholar]
  57. das S, Lohia A. Delinking of S phase and cytokinesis in the protozoan parasite Entamoeba histolytica. Cell Microbiol 2002; 4: 55– 60 [CrossRef]
    [Google Scholar]
  58. Morgado P, Manna D, Singh U. Recent advances in Entamoeba biology: RNA interference, drug discovery, and gut microbiome. F1000Res 2016; 5: 2578 [CrossRef]
    [Google Scholar]
  59. Kaur G, Lohia A. Inhibition of gene expression with double strand RNA interference in Entamoeba histolytica. Biochem Biophys Res Commun 2004; 320: 1118– 1122 [CrossRef]
    [Google Scholar]
  60. Zhang H, Pompey JM, Singh U. RNA interference in Entamoeba histolytica : implications for parasite biology and gene silencing. Future Microbiol 2011; 6: 103– 117 [CrossRef]
    [Google Scholar]
  61. Joslin CE, Tu EY, Shoff ME, Booton GC, Fuerst PA et al. The association of contact lens solution use and Acanthamoeba keratitis. Am J Ophthalmol 2007; 144: 169– 180 [CrossRef]
    [Google Scholar]
  62. Król-Turmińska K, Olender A. Human infections caused by free-living amoebae. AAEM 2017; 24: 254– 260
    [Google Scholar]
  63. Bhagwandeen SB, F.Carter R, Naik KG, Levitt D. A case of hartmannellid amebic meningoencephalitis in Zambia. Am J Clin Pathol 1975; 63: 483– 492 [CrossRef]
    [Google Scholar]
  64. Page MA, Mathers WD. Acanthamoeba keratitis: a 12-year experience covering a wide spectrum of presentations, diagnoses, and outcomes. J Ophthalmol 2013; 2013: 1– 6 [CrossRef]
    [Google Scholar]
  65. Reddy AK, Balne PK, Garg P, Sangwan VS, das M et al. Dictyostelium polycephalum Infection of Human Cornea. Emerg Infect Dis 2010; 16: 1644– 1645 [CrossRef]
    [Google Scholar]
  66. Cordingley JS, Willis RA, Villemez CL. Osmolarity is an independent trigger of Acanthamoeba castellanii differentiation. J Cell Biochem 1996; 61: 167– 171 [CrossRef]
    [Google Scholar]
  67. Aqeel Y, Siddiqui R, Iftikhar H, Khan NA. The effect of different environmental conditions on the encystation of Acanthamoeba castellanii belonging to the T4 genotype. Exp Parasitol 2013; 135: 30– 35 [CrossRef]
    [Google Scholar]
  68. Moon E-K, Kong H-H. Short-cut pathway to synthesize cellulose of encysting acanthamoeba. Korean J Parasitol 2012; 50: 361– 364 [CrossRef]
    [Google Scholar]
  69. Lorenzo-Morales J, Kliescikova J, Martinez-Carretero E, de Pablos LM, Profotova B et al. Glycogen phosphorylase in Acanthamoeba spp.: determining the role of the enzyme during the encystment process using RNA interference. Eukaryot Cell 2008; 7: 509– 517 [CrossRef]
    [Google Scholar]
  70. Aqeel Y, Siddiqui R, Khan NA. Silencing of xylose isomerase and cellulose synthase by siRNA inhibits encystation in Acanthamoeba castellanii. Parasitol Res 2013; 112: 1221– 1227 [CrossRef]
    [Google Scholar]
  71. Moon E-K, Hong Y, Chung D-I, Goo Y-K, Kong H-H. Down-regulation of cellulose synthase inhibits the formation of endocysts in acanthamoeba. Korean J Parasitol 2014; 52: 131– 135 [CrossRef]
    [Google Scholar]
  72. Moon E-K, Hong Y, Chung D-I, Goo Y-K, Kong H-H. Potential value of cellulose synthesis inhibitors combined with phmb in the treatment of Acanthamoeba keratitis. Cornea 2015; 34: 1593– 1598 [CrossRef]
    [Google Scholar]
  73. Jha BK, Jung H-J, Seo I, Kim HA, Suh S-I et al. Chloroquine has a cytotoxic effect on acanthamoeba encystation through modulation of autophagy. Antimicrob Agents Chemother 2014; 58: 6235– 6241 [CrossRef]
    [Google Scholar]
  74. Moon E-K, Kim S-H, Hong Y, Chung D-I, Goo Y-K et al. Autophagy inhibitors as a potential antiamoebic treatment for Acanthamoeba keratitis. Antimicrob Agents Chemother 2015; 59: 4020– 4025 [CrossRef]
    [Google Scholar]
  75. Moon E-K, Hong Y, Chung D-I, Kong H-H. Identification of atg8 isoform in encysting acanthamoeba. Korean J Parasitol 2013; 51: 497– 502 [CrossRef]
    [Google Scholar]
  76. Kim S-H, Moon E-K, Hong Y, Chung D-I, Kong H-H. Autophagy protein 12 plays an essential role in Acanthamoeba encystation. Exp Parasitol 2015; 159: 46– 52 [CrossRef]
    [Google Scholar]
  77. Song S-M, Han B-I, Moon E-K, Lee Y-R, Yu HS, Hs Y et al. Autophagy protein 16-mediated autophagy is required for the encystation of Acanthamoeba castellanii. Mol Biochem Parasitol 2012; 183: 158– 165 [CrossRef]
    [Google Scholar]
  78. Lee J-Y, Song S-M, Moon E-K, Lee Y-R, Jha BK et al. Cysteine protease inhibitor (AcStefin) is required for complete cyst formation of acanthamoeba. Eukaryot Cell 2013; 12: 567– 574 [CrossRef]
    [Google Scholar]
  79. Moon E-K, Hong Y, Chung D-I, Kong H-H. Cysteine protease involving in autophagosomal degradation of mitochondria during encystation of Acanthamoeba. Mol Biochem Parasitol 2012; 185: 121– 126 [CrossRef]
    [Google Scholar]
  80. Lee Y-R, Na B-K, Moon E-K, Song S-M, Joo S-Y et al. Essential role for an m17 leucine aminopeptidase in encystation of Acanthamoeba castellanii. PLoS One 2015; 10: e0129884 [CrossRef]
    [Google Scholar]
  81. Moon E-K, Hong Y, Chung D-I, Goo Y-K, Kong H-H. Identification of protein arginine methyltransferase 5 as a regulator for encystation of Acanthamoeba. Korean J Parasitol 2016; 54: 133– 138 [CrossRef]
    [Google Scholar]
  82. Moon E-K, Chung D-I, Hong Y, Kong H-H. Expression levels of encystation mediating factors in fresh strain of Acanthamoeba castellanii cyst ESTs. Exp Parasitol 2011; 127: 811– 816 [CrossRef]
    [Google Scholar]
  83. Moon E-K, Chung D-I, Hong Y-C, Kong H-H. Differentially expressed genes of Acanthamoeba castellanii during encystation. Korean J Parasitol 2007; 45: 283– 285 [CrossRef]
    [Google Scholar]
  84. Moon E-K, Xuan Y-H, Chung D-I, Hong Y, Kong H-H. Microarray analysis of differentially expressed genes between cysts and trophozoites of Acanthamoeba castellanii. Korean J Parasitol 2011; 49: 341– 347 [CrossRef]
    [Google Scholar]
  85. Achar S, Weisman R. Adenylate cyclase activity during growth and encystment of Acanthamoeba castellanii. Biochim Biophys Acta 1980; 629: 225– 234 [CrossRef]
    [Google Scholar]
  86. Chlapowski FJ, Butcher RW. Activation of adenylate cyclase in Acanthamoeba palestinensis. Life Sci 1986; 38: 849– 859 [Crossref]
    [Google Scholar]
  87. Raizada MK, Murti CRK. Transformation of trophic Hartmannella Culbertsoni into viable cysts by cyclic 3',5'-adenosine monophosphate. J Cell Biol 1972; 52: 743– 748 [CrossRef]
    [Google Scholar]
  88. Aqeel Y, Siddiqui R, Manan Z, Khan NA. The role of G protein coupled receptor-mediated signaling in the biological properties of Acanthamoeba castellanii of the T4 genotype. Microb Pathog 2015; 81: 22– 27 [CrossRef]
    [Google Scholar]
  89. Clarke M, Lohan AJ, Liu B, Lagkouvardos I, Roy S et al. Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol 2013; 14: R11 [CrossRef]
    [Google Scholar]
  90. Moon E-K, Chung D-I, Hong Y, Kong H-H. Protein kinase C signaling molecules regulate encystation of Acanthamoeba. Exp Parasitol 2012; 132: 524– 529 [CrossRef]
    [Google Scholar]
  91. Loomis WF. Cell signaling during development of Dictyostelium. Dev Biol 2014; 391: 1– 16 [CrossRef]
    [Google Scholar]
  92. Schaap P. Evolution of developmental signalling in Dictyostelid social amoebas. Curr Opin Genet Dev 2016; 39: 29– 34 [CrossRef]
    [Google Scholar]
  93. Attwood PV. Histidine kinases from bacteria to humans. Biochem Soc Trans 2013; 41: 1023– 1028 [CrossRef]
    [Google Scholar]
  94. Shaulsky G, Escalante R, Loomis WF. Developmental signal transduction pathways uncovered by genetic suppressors. Proc Natl Acad Sci USA 1996; 93: 15260– 15265 [CrossRef]
    [Google Scholar]
  95. Thomason PA, Traynor D, Stock JB, Kay RR. The RdeA-RegA system, a eukaryotic phospho-relay controlling cAMP breakdown. J Biol Chem 1999; 274: 27379– 27384 [CrossRef]
    [Google Scholar]
  96. Singleton CK, Zinda MJ, Mykytka B, Yang P. The histidine kinase dhkC regulates the choice between migrating slugs and terminal differentiation in Dictyostelium discoideum. Dev Biol 1998; 203: 345– 357 [CrossRef]
    [Google Scholar]
  97. Anjard C, Loomis WF. Peptide signaling during terminal differentiation of Dictyostelium. Proc Natl Acad Sci USA 2005; 102: 7607– 7611 [CrossRef]
    [Google Scholar]
  98. Ritchie AV, van Es S, Fouquet C, Schaap P. From drought sensing to developmental control: evolution of cyclic AMP signaling in social amoebas. Mol Biol Evol 2008; 25: 2109– 2118 [CrossRef]
    [Google Scholar]
  99. Kawabe Y, Schilde C, Du Q, Schaap P. A conserved signalling pathway for amoebozoan encystation that was co-opted for multicellular development. Sci Rep 2015; 5: 9644 [CrossRef]
    [Google Scholar]
  100. Du Q, Schilde C, Birgersson E, Chen ZH, McElroy S et al. The cyclic AMP phosphodiesterase RegA critically regulates encystation in social and pathogenic amoebas. Cell Signal 2014; 26: 453– 459 [CrossRef] [PubMed]
    [Google Scholar]
  101. Du Q, Schaap P. The social amoeba Polysphondylium pallidum loses encystation and sporulation, but can still erect fruiting bodies in the absence of cellulose. Protist 2014; 165: 569– 579 [CrossRef] [PubMed]
    [Google Scholar]
  102. Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R et al. The genome of the social amoeba Dictyostelium discoideum. Nature 2005; 435: 43– 57 [CrossRef] [PubMed]
    [Google Scholar]
  103. Schaap P, Barrantes I, Minx P, Sasaki N, Anderson RW et al. The Physarum polycephalum genome reveals extensive use of prokaryotic two-component and metazoan-type tyrosine kinase signaling. Genome Biol Evol 2015; 8: 109– 125 [CrossRef] [PubMed]
    [Google Scholar]
  104. Saran S, Schaap P. Adenylyl cyclase G is activated by an intramolecular osmosensor. Mol Biol Cell 2004; 15: 1479– 1486 [CrossRef] [PubMed]
    [Google Scholar]
  105. Krabberød AK, Orr RJS, Bråte J, Kristensen T, Bjørklund KR et al. Single cell transcriptomics, mega-phylogeny, and the genetic basis of morphological innovations in rhizaria. Mol Biol Evol 2017; 34: 1557– 1573 [CrossRef] [PubMed]
    [Google Scholar]
  106. Microworld 2016; World of amoeboid organisms [database on the Internet]. www.arcella.nl
  107. Du Q, Kawabe Y, Schilde C, Chen ZH, Schaap P. The evolution of aggregative multicellularity and cell-cell communication in the Dictyostelia. J Mol Biol 2015; 427: 3722– 3733 [CrossRef] [PubMed]
    [Google Scholar]
  108. Goldberg JM, Manning G, Liu A, Fey P, Pilcher KE et al. The dictyostelium kinome-analysis of the protein kinases from a simple model organism. PLoS Genet 2006; 2: e38 303 [CrossRef] [PubMed]
    [Google Scholar]
  109. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 2010; 140: 631– 642 [CrossRef] [PubMed]
    [Google Scholar]
  110. Anamika K, Bhattacharya A, Srinivasan N. Analysis of the protein kinome of Entamoeba histolytica. Proteins 2008; 71: 995– 1006 [CrossRef] [PubMed]
    [Google Scholar]
  111. Picazarri K, Luna-Arias JP, Carrillo E, Orozco E, Rodriguez MA. Entamoeba histolytica: identification of EhGPCR-1, a novel putative G protein-coupled receptor that binds to EhRabB. Exp Parasitol 2005; 110: 253– 258 [CrossRef] [PubMed]
    [Google Scholar]
  112. Bosch DE, Kimple AJ, Muller RE, Giguère PM, Machius M et al. Heterotrimeric G-protein signaling is critical to pathogenic processes in Entamoeba histolytica. PLoS Pathog 2012; 8: e1003040 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000653
Loading
/content/journal/micro/10.1099/mic.0.000653
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error