Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Differentially Expressed Gene Profile of Acanthamoeba castellanii Induced by an Endosymbiont Legionella pneumophila

  • Moon, Eun-Kyung (Department of Medical Zoology, Kyung Hee University School of Medicine) ;
  • Park, So-Min (Department of Biomedical Science, Graduate School, Kyung Hee University) ;
  • Chu, Ki-Back (Department of Biomedical Science, Graduate School, Kyung Hee University) ;
  • Quan, Fu-Shi (Department of Medical Zoology, Kyung Hee University School of Medicine) ;
  • Kong, Hyun-Hee (Department of Parasitology, Dong-A University College of Medicine)
  • Received : 2020.10.14
  • Accepted : 2020.12.21
  • Published : 2021.02.28
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Abstract

Legionella pneumophila is an opportunistic pathogen that survives and proliferates within protists such as Acanthamoeba spp. in environment. However, intracellular pathogenic endosymbiosis and its implications within Acanthamoeba spp. remain poorly understood. In this study, RNA sequencing analysis was used to investigate transcriptional changes in A. castellanii in response to L. pneumophila infection. Based on RNA sequencing data, we identified 1,211 upregulated genes and 1,131 downregulated genes in A. castellanii infected with L. pneumophila for 12 hr. After 24 hr, 1,321 upregulated genes and 1,379 downregulated genes were identified. Gene ontology (GO) analysis revealed that L. pneumophila endosymbiosis enhanced hydrolase activity, catalytic activity, and DNA binding while reducing oxidoreductase activity in the molecular function (MF) domain. In particular, multiple genes associated with the GO term 'integral component of membrane' were downregulated during endosymbiosis. The endosymbiont also induced differential expression of various methyltransferases and acetyltransferases in A. castellanii. Findings herein are may significantly contribute to understanding endosymbiosis of L. pneumophila within A. castellanii.

Keywords

References

  1. Visvesvara GS, Moura H, Schuster FL. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol 2007; 50: 1-26. https://doi.org/10.1111/j.1574-695X.2007.00232.x
  2. Schmitz-Esser S, Toenshoff ER, Haider S, Heinz E, Hoenninger VM, Wagner M, Horn M. Diversity of bacterial endosymbionts of environmental Acanthamoeba isolates. Appl Environ Microbiol 2008; 74: 5822-5831. https://doi.org/10.1128/AEM.01093-08
  3. Greub G, Raoult D. Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 2004; 17: 413-433. https://doi.org/10.1128/cmr.17.2.413-433.2004
  4. Richards AM, Von Dwingelo JE, Price CT, Abu Kwaik Y. Cellular microbiology and molecular ecology of Legionella-amoeba interaction. Virulence 2013; 4: 307-314. https://doi.org/10.4161/viru.24290
  5. Barker J, Brown MR. Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 1994; 140: 1253-1259. https://doi.org/10.1099/00221287-140-6-1253
  6. Essig A, Heinemann M, Simnacher U, Marre R. Infection of Acanthamoeba castellanii by Chlamydia pneumoniae. Appl Environ Microbiol 1997; 63: 1396-1399. https://doi.org/10.1128/AEM.63.4.1396-1399.1997
  7. Guimaraes AJ, Gomes KX, Cortines JR, Peralta JM, Peralta RH. Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence. Microbiol Res 2016; 193: 30-38. https://doi.org/10.1016/j.micres.2016.08.001
  8. Isberg RR, O'Connor TJ, Heidtman M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 2009; 7: 13-24. https://doi.org/10.1038/nrmicro1967
  9. Vogel JP, Andrews HL, Wong SK, Isberg RR. Conjugative transfer by the virulence system of Legionella pneumophila. Science 1998; 279: 873-876. https://doi.org/10.1126/science.279.5352.873
  10. Steiner B, Weber S, Hilbi H. Formation of the Legionella-containing vacuole: phosphoinositide conversion, GTPase modulation and ER dynamics. Int J Med Microbiol 2018; 308: 49-57. https://doi.org/10.1016/j.ijmm.2017.08.004
  11. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, Ma L, Tichit M, Jarraud S, Bouchier C, Vandenesch F, Kunst F, Etienne J, Glaser P, Buchrieser C. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 2004; 36: 1165-1173. https://doi.org/10.1038/ng1447
  12. Cazalet C, Gomez-Valero L, Rusniok C, Lomma M, Dervins-Ravault D, Newton HJ, Sansom FM, Jarraud S, Zidane N, Ma L, Bouchier C, Etienne J, Hartland EL, Buchrieser C. Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet 2010; 6: e1000851. https://doi.org/10.1371/journal.pgen.1000851
  13. Molmeret M, Bitar DM, Han L, Kwaik YA. Disruption of the phagosomal membrane and egress of Legionella pneumophila into the cytoplasm during the last stages of intracellular infection of macrophages and Acanthamoeba polyphaga. Infect Immun 2004; 72: 4040-4051. https://doi.org/10.1128/IAI.72.7.4040-4051.2004
  14. Mou Q, Leung PHM. Differential expression of virulence genes in Legionella pneumophila growing in Acanthamoeba and human monocytes. Virulence 2018; 9: 185-196. https://doi.org/10.1080/21505594.2017.1373925
  15. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009; 25: 1105-1111. https://doi.org/10.1093/bioinformatics/btp120
  16. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26: 841-842. https://doi.org/10.1093/bioinformatics/btq033
  17. Varet H, Brillet-Gueguen L, Coppee JY, Dillies MA. SARTools: A DESeq2- and EdgeR-Based R Pipeline for Comprehensive Differential Analysis of RNA-Seq Data. PLoS One 2016; 11: e0157022. https://doi.org/10.1371/journal.pone.0157022
  18. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80. https://doi.org/10.1186/gb-2004-5-10-r80
  19. Qiu J, Luo ZQ. Legionella and Coxiella effectors: strength in diversity and activity. Nat Rev Microbiol 2017; 15: 591-605. https://doi.org/10.1038/nrmicro.2017.67
  20. Yen CY, Huang HW, Shu CW, Hou MF, Yuan SS, Wang HR, Chang YT, Farooqi AA, Tang JY, Chang HW. DNA methylation, histone acetylation and methylation of epigenetic modifications as a therapeutic approach for cancers. Cancer Lett 2016; 373: 185-192. https://doi.org/10.1016/j.canlet.2016.01.036

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