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Diversity profiling of xenic cultures of Dientamoeba fragilis following systematic antibiotic treatment and prospects for genome sequencing

Published online by Cambridge University Press:  23 September 2019

Rory Gough*
Affiliation:
The University of Technology Sydney, Australia St Vincent's Hospital, Sydney, Australia
Joel Barratt
Affiliation:
The University of Technology Sydney, Australia
Damien Stark
Affiliation:
The University of Technology Sydney, Australia St Vincent's Hospital, Sydney, Australia
John Ellis
Affiliation:
The University of Technology Sydney, Australia
*
Author for correspondence: Rory Gough, E-mail: rory.c.gough@student.uts.edu.au

Abstract

The presence of bacterial DNA in Dientamoeba fragilis DNA extracts from culture poses a substantial challenge to sequencing the D. fragilis genome. However, elimination of bacteria from D. fragilis cultures has proven difficult in the past, presumably due to its dependence on some unknown prokaryote/s. This study explored options for removal of bacteria from D. fragilis cultures and for the generation of genome sequence data from D. fragilis. DNA was extracted from human faecal samples and xenic D. fragilis cultures. Extracts were subjected to 16S ribosomal DNA bacterial diversity profiling. Xenic D. fragilis cultures were then subject to antibiotic treatment regimens that systematically removed bacterial species depending on their membrane structure (Gram-positive or Gram-negative) and aerobic requirements. The impact of these treatments on cultures was assessed by 16S amplicon sequencing. Prior to antibiotic treatment, the cultures were dominated by Gram-negative bacteria. Addition of meropenem to cultures eliminated anaerobic Gram-negative bacteria, but it also led to protozoan death after 5 days incubation. The seeding of meropenem resistant Klebsiella pneumoniae strain KPC-2 into cultures before treatment by meropenem prevented death of D. fragilis cells beyond this 5 day period, suggesting that one or more species of Gram-negative bacteria may be an essential nutritional requirement for D. fragilis. Gram-positive cells were completely eliminated using vancomycin without affecting trophozoite growth. Finally, this study shows that genome sequencing of D. fragilis is feasible following bacterial elimination from cultures as the result of the major advances occurring in bioinformatics. We provide evidence on this fact by successfully sequencing the D. fragilis 28S large ribosomal DNA subunit gene using culture-derived DNA.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019

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References

Arumugam, M, Raes, J, Pelletier, E, Le Paslier, D, Yamada, T, Mende, DR, Fernandes, GR, Tap, J, Bruls, T, Batto, J-M, Bertalan, M, Borruel, N, Casellas, F, Fernandez, L, Gautier, L, Hansen, T, Hattori, M, Hayashi, T, Kleerebezem, M, Kurokawa, K, Leclerc, M, Levenez, F, Manichanh, C, Nielsen, HB, Nielsen, T, Pons, N, Poulain, J, Qin, J, Sicheritz-Ponten, T, Tims, S, Torrents, D, Ugarte, E, Zoetendal, EG, Wang, J, Guarner, F, Pedersen, O, de Vos, WM, Brunak, S, Doré, J, Meta, HITC, Antolín, M, Artiguenave, F, Blottiere, HM, Almeida, M, Brechot, C, Cara, C, Chervaux, C, Cultrone, A, Delorme, C, Denariaz, G, Dervyn, R, Foerstner, KU, Friss, C, van de Guchte, M, Guedon, E, Haimet, F, Huber, W, van Hylckama-Vlieg, J, Jamet, A, Juste, C, Kaci, G, Knol, J, Kristiansen, K, Lakhdari, O, Layec, S, Le Roux, K, Maguin, E, Mérieux, A, Melo Minardi, R, M'Rini, C, Muller, J, Oozeer, R, Parkhill, J, Renault, P, Rescigno, M, Sanchez, N, Sunagawa, S, Torrejon, A, Turner, K, Vandemeulebrouck, G, Varela, E, Winogradsky, Y, Zeller, G, Weissenbach, J, Ehrlich, SD and Bork, P (2011) Enterotypes of the human gut microbiome. Nature 473, 174.CrossRefGoogle ScholarPubMed
Balamuth, W (1946) Improved egg yolk infusion for cultivation of Entamoeba histolytica and other intestinal protozoa. American Journal of Clinical Pathology 16, 380384.CrossRefGoogle ScholarPubMed
Bär, A-K, Phukan, N, Pinheiro, J and Simoes-Barbosa, A (2015) The interplay of host Microbiota and parasitic protozoans at mucosal interfaces: implications for the outcomes of infections and diseases. PLOS Neglected Tropical Diseases 9, e0004176.CrossRefGoogle ScholarPubMed
Barratt, JLN, Banik, GR, Harkness, J, Marriott, D, Ellis, JT and Stark, D (2010) Newly defined conditions for the in vitro cultivation and cryopreservation of Dientamoeba fragilis: new techniques set to fast track molecular studies on this organism. Parasitology 137, 18671878.CrossRefGoogle ScholarPubMed
Barratt, JL, Harkness, J, Marriott, D, Ellis, JT and Stark, D (2011) A review of Dientamoeba fragilis carriage in humans: several reasons why this organism should be considered in the diagnosis of gastrointestinal illness. Gut Microbes 2, 312.CrossRefGoogle Scholar
Barratt, JLN, Cao, M, Stark, DJ and Ellis, JT (2015) The transcriptome sequence of Dientamoeba fragilis offers new biological insights on its metabolism, kinome, degradome and potential mechanisms of pathogenicity. Protist 166, 389408.CrossRefGoogle ScholarPubMed
Barratt, J, Gough, R, Stark, D and Ellis, J (2016) Bulky trichomonad genomes: encoding a Swiss Army Knife. Trends in Parasitology 32, 783797.CrossRefGoogle ScholarPubMed
Brug, SL (1936) Observations on Dientamoeba fragilis. Annals of Tropical Medicine and Parasitology 30, 441452.CrossRefGoogle Scholar
Bull, MJ and Plummer, NT (2014) Part 1: The human gut microbiome in health and disease. Integrative Medicine: A Clinician's Journal 13, 1722.Google ScholarPubMed
Caesar, R, Tremaroli, V, Kovatcheva-Datchary, P, Cani, PD and Bäckhed, F (2015) Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metabolism 22, 658668.CrossRefGoogle ScholarPubMed
Carlton, JM, Hirt, RP, Silva, JC, Delcher, AL, Schatz, M, Zhao, Q, Wortman, JR, Bidwell, SL, Alsmark, UCM, Besteiro, S, Sicheritz-Ponten, T, Noel, CJ, Dacks, JB, Foster, PG, Simillion, C, Van de Peer, Y, Miranda-Saavedra, D, Barton, GJ, Westrop, GD, Müller, S, Dessi, D, Fiori, PL, Ren, Q, Paulsen, I, Zhang, H, Bastida-Corcuera, FD, Simoes-Barbosa, A, Brown, MT, Hayes, RD, Mukherjee, M, Okumura, CY, Schneider, R, Smith, AJ, Vanacova, S, Villalvazo, M, Haas, BJ, Pertea, M, Feldblyum, TV, Utterback, TR, Shu, C-L, Osoegawa, K, de Jong, PJ, Hrdy, I, Horvathova, L, Zubacova, Z, Dolezal, P, Malik, S-B, Logsdon, JM Jr., Henze, K, Gupta, A, Wang, CC, Dunne, RL, Upcroft, JA, Upcroft, P, White, O, Salzberg, SL, Tang, P, Chiu, C-H, Lee, Y-S, Embley, TM, Coombs, GH, Mottram, JC, Tachezy, J, Fraser-Liggett, CM and Johnson, PJ (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science (New York) 315, 207212.CrossRefGoogle ScholarPubMed
Chan, D, Barratt, J, Roberts, T, Phillips, O, Šlapeta, J, Ryan, U, Marriott, D, Harkness, J, Ellis, J and Stark, D (2016) Detection of Dientamoeba fragilis in animal faeces using species specific real time PCR assay. Veterinary Parasitology 227, 4247.CrossRefGoogle ScholarPubMed
Chan, FT, Guan, MX and Mackenzie, AM (1993) Application of indirect immunofluorescence to detection of Dientamoeba fragilis trophozoites in fecal specimens. Journal of Clinical Microbiology 31, 17101714.CrossRefGoogle ScholarPubMed
Chan, FT, Guan, MX, Mackenzie, AM and Diaz-Mitoma, F (1994) Susceptibility testing of Dientamoeba fragilis ATCC 30948 with iodoquinol, paromomycin, tetracycline, and metronidazole. Antimicrobial Agents and Chemotherapy 38, 1157.CrossRefGoogle ScholarPubMed
Dicksved, J, Halfvarson, J, Rosenquist, M, Jarnerot, G, Tysk, C, Apajalahti, J, Engstrand, L and Jansson, JK (2008) Molecular analysis of the gut microbiota of identical twins with Crohn's disease. The ISME Journal 2, 716727.CrossRefGoogle ScholarPubMed
Dwyer, DM and Honigber, BM (1971) Freezing and maintenance of Dientamoeba fragilis in liquid nitrogen. Journal of Parasitology 57, 190–19&.CrossRefGoogle Scholar
Eckburg, PB, Bik, EM, Bernstein, CN, Purdom, E, Dethlefsen, L, Sargent, M, Gill, SR, Nelson, KE and Relman, DA (2005) Diversity of the human intestinal microbial flora. Science 308, 16351638.CrossRefGoogle ScholarPubMed
Giske, CG, Martinez-Martinez, L, Canton, R, Stefani, S, Skov, R, Glupczynski, Y, Nordmann, PN, Wootton, M, Miriagou, V, Simonsen, GS, Zemlickova, H, Cohen-Stuart, J and Gniadkowski, M (2017) EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. Version 2.0. European Committee on Antimicrobial Susceptibility Testing.Google Scholar
Gough, R, Ellis, J and Stark, D (2019) Comparison and recommendations for use of Dientamoeba fragilis real-time PCR assays. Journal of Clinical Microbiology 57, e01466e01418.CrossRefGoogle ScholarPubMed
Hammer, O, Harper, D and Ryan, P (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 9, http://palaeo-electronica.org/2001_1/past/issue1_01.htmGoogle Scholar
Harris, MA, Reddy, CA and Carter, GR (1976) Anaerobic bacteria from the large intestine of mice. Applied and Environmental Microbiology 31, 907912.CrossRefGoogle Scholar
Holt, KE, Schultz, MB, Wick, RR and Zobel, J (2015) Bandage: interactive visualization of de novo genome assemblies. Bioinformatics (Oxford, England) 31, 33503352.Google Scholar
Hugenholtz, P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biology 3, reviews0003.0001reviews0003.0008.CrossRefGoogle ScholarPubMed
Hugon, P, Dufour, JC, Colson, P, Fournier, PE, Sallah, K and Raoult, D (2015) A comprehensive repertoire of prokaryotic species identified in human beings. The Lancet Infectious Diseases 15, 12111219.CrossRefGoogle ScholarPubMed
Jacobs, L (1953) The cultivation of Dientamoeba fragilis. Annals of the New York Academy of Sciences 56, 10571061.CrossRefGoogle Scholar
Jokelainen, P, Hebbelstrup Jensen, B, Andreassen, BU, Petersen, AM, Roser, D, Krogfelt, KA, Nielsen, HV and Stensvold, CR (2017) Dientamoeba fragilis, a commensal in children in Danish day care centers. Journal of Clinical Microbiology 55, 17071713.CrossRefGoogle ScholarPubMed
Leung, JM, Graham, AL and Knowles, SCL (2018) Parasite-microbiota interactions with the vertebrate gut: synthesis through an ecological lens. Frontiers in microbiology 9, 843843.CrossRefGoogle ScholarPubMed
Ley, RE, Turnbaugh, PJ, Klein, S and Gordon, JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444, 10221023.CrossRefGoogle ScholarPubMed
Lozupone, CA, Stombaugh, JI, Gordon, JI, Jansson, JK and Knight, R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489, 220230.CrossRefGoogle ScholarPubMed
Moss, T and Stefanovsky, VY (1995) Promotion and regulation of ribosomal transcription in eukaryotes by RNA polymerase I. Prog Nucleic Acid Res Mol Biol. 50, 2566.CrossRefGoogle Scholar
Munasinghe, VS, Stark, D and Ellis, JT (2012) New advances in the in vitro culture of Dientamoeba fragilis. Parasitology 139, 864869.CrossRefGoogle ScholarPubMed
Munasinghe, VS, Vella, NGF, Ellis, JT, Windsor, PA and Stark, D (2013) Cyst formation and faecal-oral transmission of Dientamoeba fragilis – the missing link in the life cycle of an emerging pathogen. International Journal for Parasitology 43, 879883.CrossRefGoogle ScholarPubMed
Nagata, N, Marriott, D, Harkness, J, Ellis, JT and Stark, D (2012) In vitro susceptibility testing of Dientamoeba fragilis. Antimicrobial Agents and Chemotherapy 56, 487.CrossRefGoogle ScholarPubMed
Nurk, S, Meleshko, D, Korobeynikov, A and Pevzner, PA (2017) metaSPAdes: a new versatile metagenomic assembler. Genome research 27, 824834.CrossRefGoogle ScholarPubMed
O'Brien Andersen, L, Karim, AB, Roager, HM, Vigsnæs, LK, Krogfelt, KA, Licht, TR and Stensvold, CR (2016) Associations between common intestinal parasites and bacteria in humans as revealed by qPCR. European Journal of Clinical Microbiology & Infectious Diseases 35, 14271431.CrossRefGoogle ScholarPubMed
Partida-Rodriguez, O, Serrano-Vazquez, A, Nieves-Ramirez, ME, Moran, P, Rojas, L, Portillo, T, Gonzalez, E, Hernandez, E, Finlay, BB and Ximenez, C (2017) Human intestinal microbiota: interaction between parasites and the host immune response. Archives of Medical Research 48, 690700.CrossRefGoogle ScholarPubMed
Roy, S and Trinchieri, G (2017) Microbiota: a key orchestrator of cancer therapy. Nature Reviews Cancer 17, 271.CrossRefGoogle ScholarPubMed
Sawangjaroen, N, Luke, R and Prociv, P (1993) Diagnosis by faecal culture of Dientamoeba fragilis infections in Australian patients with diarrhoea. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 163165.CrossRefGoogle ScholarPubMed
Sekirov, I, Russell, SL, Antunes, LC and Finlay, BB (2010) Gut microbiota in health and disease. Physiological reviews 90, 859904.CrossRefGoogle ScholarPubMed
Sheikh, W, Pitkin, DH and Nadler, H (1993) Antibacterial activity of meropenem and selected comparative agents against anaerobic bacteria at seven North American centers. Journal of Biochemistry and Molecular Biology, 16(Suppl. 4), S361S366.Google ScholarPubMed
Srivastava, AK and Schlessinger, D (1991) Structure and organization of ribosomal DNA. Biochimie 73, 631638.CrossRefGoogle ScholarPubMed
Stark, D, Roberts, T, Ellis, JT, Marriott, D and Harkness, J (2014) Evaluation of the EasyScreen enteric parasite detection kit for the detection of Blastocystis spp., Cryptosporidium spp., Dientamoeba fragilis, Entamoeba complex, and Giardia intestinalis from clinical stool samples. Diagnostic Microbiology and Infectious Disease 78, 149152.CrossRefGoogle Scholar
Stark, D, Barratt, J, Chan, D and Ellis, JT (2016) Dientamoeba fraiglis, the neglected trichomonad of the human bowel. Clinical Microbiology Reviews 29, 553.CrossRefGoogle Scholar
Tringe, SG, von Mering, C, Kobayashi, A, Salamov, AA, Chen, K, Chang, HW, Podar, M, Short, JM, Mathur, EJ, Detter, JC, Bork, P, Hugenholtz, P and Rubin, EM (2005) Comparative metagenomics of microbial communities. Science 308, 554557.CrossRefGoogle ScholarPubMed
van Passel, MWJ, Kant, R, Zoetendal, EG, Plugge, CM, Derrien, M, Malfatti, SA, Chain, PSG, Woyke, T, Palva, A, de Vos, WM and Smidt, H (2011) The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLOS ONE 6, e16876.CrossRefGoogle ScholarPubMed
Villegas, MV, Lolans, K, Correa, A, Suarez, CJ, Lopez, JA, Vallejo, M and Quinn, JP (2006) First detection of the plasmid-mediated class A carbapenemase KPC-2 in clinical isolates of Klebsiella pneumoniae from South America. Antimicrobial Agents and Chemotherapy 50, 28802882.CrossRefGoogle Scholar
Watanakunakorn, C (1981) The antibacterial action of vancomycin. Reviews of Infectious Diseases, 3(Suppl.), S210S215.CrossRefGoogle ScholarPubMed
Wiseman, LR, Wagstaff, AJ, Brogden, RN and Bryson, HM (1995) Meropenem. A review of its antibacterial activity, pharmacokinetic properties and clinical efficacy. Drugs 50, 73101.CrossRefGoogle ScholarPubMed
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