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European Journal of Clinical Microbiology & Infectious Diseases

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01-10-2016 | Original Article

Whole genome sequencing as a tool for phylogenetic analysis of clinical strains of Mitis group streptococci

Authors: L. H. Rasmussen, R. Dargis, K. Højholt, J. J. Christensen, O. Skovgaard, U. S. Justesen, F. S. Rosenvinge, C. Moser, O. Lukjancenko, S. Rasmussen, X. C. Nielsen

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 10/2016

Abstract

Identification of Mitis group streptococci (MGS) to the species level is challenging for routine microbiology laboratories. Correct identification is crucial for the diagnosis of infective endocarditis, identification of treatment failure, and/or infection relapse. Eighty MGS from Danish patients with infective endocarditis were whole genome sequenced. We compared the phylogenetic analyses based on single genes (recA, sodA, gdh), multigene (MLSA), SNPs, and core-genome sequences. The six phylogenetic analyses generally showed a similar pattern of six monophyletic clusters, though a few differences were observed in single gene analyses. Species identification based on single gene analysis showed their limitations when more strains were included. In contrast, analyses incorporating more sequence data, like MLSA, SNPs and core-genome analyses, provided more distinct clustering. The core-genome tree showed the most distinct clustering.

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Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43(11):5721–5732. doi:10.1128/JCM.43.11.5721-5732.2005 PubMedPubMedCentralCrossRef

Smith DJ, Anderson JM, King WF, Van HJ, Taubman MA (1993) Oral streptococcal colonization of infants. Oral Microbiol Immunol 8(1):1–4PubMedCrossRef

Kilian M, Poulsen K, Blomqvist T, Havarstein LS, Bek-Thomsen M, Tettelin H, Sorensen UB (2008) Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS One 3 (7):e2683. doi:10.1371/journal.pone.0002683

Kassis H, Marnejon T, Gemmel D, Cutrona A, Gottimukkula R (2010) Streptococcus sanguinis brain abscess as complication of subclinical endocarditis: emphasizing the importance of prompt diagnosis. South Med J 103(6):559–562. doi:10.1097/SMJ.0b013e3181dfd140 PubMedCrossRef

Matthys C, Claeys G, Verschraegen G, Wauters G, Vogelaers D, De BT, Verhelst R, Van NG, Van CR, Vaneechoutte M (2006) Streptococcus cristatus isolated from a resected heart valve and blood cultures: case reports and application of phenotypic and genotypic techniques for identification. Acta Clin Belg 61(4):196–200PubMedCrossRef

Renton BJ, Clague JE, Cooke RP (2009) Streptococcus oralis endocarditis presenting as infective discitis in an edentulous patient. Int J Cardiol 137(1):e13–e14. doi:10.1016/j.ijcard.2008.05.040

Huang IF, Chiou CC, Liu YC, Hsieh KS (2002) Endocarditis caused by penicillin-resistant Streptococcus mitis in a 12-year-old boy. J Microbiol Immunol Infect 35(2):129–132PubMed

Hall GE, Baddour LM (2002) Apparent failure of endocarditis prophylaxis caused by penicillin-resistant Streptococcus mitis. Am J Med Sci 324(1):51–53PubMedCrossRef

Goud A, Abdelqader A, Dahagam C, Padmanabhan S (2015) Isolated pulmonic valve endocarditis presenting as neck pain. J Commun Hosp Intern Med Perspect 5(6):29647. doi:10.3402/jchimp.v5.29647

10.

Douglas CW, Heath J, Hampton KK, Preston FE (1993) Identity of viridans streptococci isolated from cases of infective endocarditis. J Med Microbiol 39(3):179–182. doi:10.1099/00222615-39-3-179 PubMedCrossRef

11.

Zbinden A, Mueller NJ, Tarr PE, Sproer C, Keller PM, Bloemberg GV (2012) Streptococcus tigurinus sp. nov., isolated from blood of patients with endocarditis, meningitis and spondylodiscitis. Int J Syst Evol Microbiol 62(Pt 12):2941–2945. doi:10.1099/ijs.0.038299-0 PubMedCrossRef

12.

Lopez-Pardo F, Aguilera A, Villa M, Granado C, Campos A, Cisneros JM (2004) Double-chambered right ventricle associated with mural and pulmonic valve endocarditis: description of a clinical case and review of the literature. Echocardiography 21(2):171–173PubMedCrossRef

13.

Iversen K, Host N, Bruun NE, Elming H, Pump B, Christensen JJ, Gill S, Rosenvinge F, Wiggers H, Fuursted K, Holst-Hansen C, Korup E, Schonheyder HC, Hassager C, Hofsten D, Larsen JH, Moser C, Ihlemann N, Bundgaard H (2013) Partial oral treatment of endocarditis. Am Heart J 165(2):116–122. doi:10.1016/j.ahj.2012.11.006 PubMedCrossRef

14.

Poulsen SO, Rasmussen L, Nielsen XC, Justesen US, Christensen JJ, Gill S (2015) Correct species identification of streptococcus using multi locus sequence analysis for disproving relapse of two episodes of infective endocarditis. Open Infect Dis J 9:35–38

15.

Hoshino T, Fujiwara T, Kilian M (2005) Use of phylogenetic and phenotypic analyses to identify nonhemolytic streptococci isolated from bacteremic patients. J Clin Microbiol 43(12):6073–6085. doi:10.1128/JCM.43.12.6073-6085.2005 PubMedPubMedCentralCrossRef

16.

Glazunova OO, Raoult D, Roux V (2006) Streptococcus massiliensis sp. nov., isolated from a patient blood culture. Int J Syst Evol Microbiol 56(Pt 5):1127–1131. doi:10.1099/ijs.0.64009-0 PubMedCrossRef

17.

Okamoto M, Imai S, Miyanohara M, Saito W, Momoi Y, Nomura Y, Ikawa T, Ogawa T, Miyabe-Nishiwaki T, Kaneko A, Watanabe A, Watanabe S, Hayashi M, Tomonaga M, Hanada N (2015) Streptococcus panodentis sp. nov. from the oral cavities of chimpanzees. Microbiol Immunol 59(9):526–532. doi:10.1111/1348-0421.12290 PubMedCrossRef

18.

Saito M, Shinozaki-Kuwahara N, Hirasawa M, Takada K (2016) Streptococcus oricebi sp. nov., isolated from the oral cavity of tufted capuchin. Int J Syst Evol Microbiol 66(2):1063–1067. doi:10.1099/ijsem.0.000834 PubMedCrossRef

19.

Martin V, Manes-Lazaro R, Rodriguez JM, Maldonado-Barragan A (2011) Streptococcus lactarius sp. nov., isolated from breast milk of healthy women. Int J Syst Evol Microbiol 61(Pt 5):1048–1052. doi:10.1099/ijs.0.021642-0 PubMedCrossRef

20.

Camelo-Castillo A, Benitez-Paez A, Belda-Ferre P, Cabrera-Rubio R, Mira A (2014) Streptococcus dentisani sp. nov., a novel member of the mitis group. Int J Syst Evol Microbiol 64(Pt 1):60–65. doi:10.1099/ijs.0.054098-0 PubMedCrossRef

21.

Huch M, De Bruyne K, Cleenwerck I, Bub A, Cho GS, Watzl B, Snauwaert I, Franz CM, Vandamme P (2013) Streptococcus rubneri sp. nov., isolated from the human throat. Int J Syst Evol Microbiol 63(Pt 11):4026–4032. doi:10.1099/ijs.0.048538-0 PubMedCrossRef

22.

Tong H, Gao X, Dong X (2003) Streptococcus oligofermentans sp. nov., a novel oral isolate from caries-free humans. Int J Syst Evol Microbiol 53(Pt 4):1101–1104. doi:10.1099/ijs.0.02493-0 PubMedCrossRef

23.

Whatmore AM, Efstratiou A, Pickerill AP, Broughton K, Woodard G, Sturgeon D, George R, Dowson CG (2000) Genetic relationships between clinical isolates of Streptococcus pneumoniae, Streptococcus oralis, and Streptococcus mitis: characterization of “Atypical” pneumococci and organisms allied to S. mitis harboring S. pneumoniae virulence factor-encoding genes. Infect Immun 68(3):1374–1382PubMedPubMedCentralCrossRef

24.

Isaksson J, Rasmussen M, Nilson B, Stadler LS, Kurland S, Olaison L, Ek E, Herrmann B (2015) Comparison of species identification of endocarditis associated viridans streptococci using rnpB genotyping and 2 MALDI-TOF systems. Diagn Microbiol Infect Dis 81(4):240–245. doi:10.1016/j.diagmicrobio.2014.12.007 PubMedCrossRef

25.

Kawamura Y, Hou XG, Sultana F, Miura H, Ezaki T (1995) Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int J Syst Bacteriol 45(2):406–408PubMedCrossRef

26.

Jamal W, Albert MJ, Rotimi VO (2014) Real-time comparative evaluation of bioMerieux VITEK MS versus Bruker Microflex MS, two matrix-assisted laser desorption-ionization time-of-flight mass spectrometry systems, for identification of clinically significant bacteria. BMC Microbiol 14(1):289. doi:10.1186/s12866-014-0289-0

27.

Lee M, Chung HS, Moon HW, Lee SH, Lee K (2015) Comparative evaluation of two matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) systems, Vitek MS and Microflex LT, for the identification of Gram-positive cocci routinely isolated in clinical microbiology laboratories. J Microbiol Methods 113:13–15. doi:10.1016/j.mimet.2015.03.020 PubMedCrossRef

28.

Poyart C, Quesne G, Coulon S, Berche P, Trieu-Cuot P (1998) Identification of streptococci to species level by sequencing the gene encoding the manganese-dependent superoxide dismutase. J Clin Microbiol 36(1):41–47PubMedPubMedCentral

29.

Zbinden A, Kohler N, Bloemberg GV (2011) recA-based PCR assay for accurate differentiation of Streptococcus pneumoniae from other viridans streptococci. J Clin Microbiol 49(2):523–527. doi:10.1128/JCM.01450-10 PubMedPubMedCentralCrossRef

30.

Nielsen XC, Justesen US, Dargis R, Kemp M, Christensen JJ (2009) Identification of clinically relevant nonhemolytic Streptococci on the basis of sequence analysis of 16S-23S intergenic spacer region and partial gdh gene. J Clin Microbiol 47(4):932–939. doi:10.1128/JCM.01449-08 PubMedPubMedCentralCrossRef

31.

Thompson CC, Emmel VE, Fonseca EL, Marin MA, Vicente AC (2013) Streptococcal taxonomy based on genome sequence analyses. F1000Res 2:67. doi:10.12688/f1000research.2-67.v1PubMedPubMedCentral

32.

Bosshard PP, Abels S, Altwegg M, Bottger EC, Zbinden R (2004) Comparison of conventional and molecular methods for identification of aerobic catalase-negative gram-positive cocci in the clinical laboratory. J Clin Microbiol 42(5):2065–2073PubMedPubMedCentralCrossRef

33.

Chen CC, Teng LJ, Chang TC (2004) Identification of clinically relevant viridans group streptococci by sequence analysis of the 16S-23S ribosomal DNA spacer region. J Clin Microbiol 42(6):2651–2657. doi:10.1128/JCM.42.6.2651-2657.2004 PubMedPubMedCentralCrossRef

34.

Bishop CJ, Aanensen DM, Jordan GE, Kilian M, Hanage WP, Spratt BG (2009) Assigning strains to bacterial species via the internet. BMC Biol 7:3. doi:10.1186/1741-7007-7-3

35.

Hanage WP, Fraser C, Spratt BG (2006) Sequences, sequence clusters and bacterial species. Philos Trans R Soc Lond B Biol Sci 361(1475):1917–1927. doi:10.1098/rstb.2006.1917 PubMedPubMedCentralCrossRef

36.

Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ, Angiuoli SV, Oggioni M, Dunning Hotopp JC, Hu FZ, Riley DR, Covacci A, Mitchell TJ, Bentley SD, Kilian M, Ehrlich GD, Rappuoli R, Moxon ER, Masignani V (2010) Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 11(10):R107. doi:10.1186/gb-2010-11-10-r107

37.

Kilian M, Riley DR, Jensen A, Bruggemann H, Tettelin H (2014) Parallel evolution of Streptococcus pneumoniae and Streptococcus mitis to pathogenic and mutualistic lifestyles. MBio 5(4):e01490–01414. doi:10.1128/mBio.01490-14

38.

Lukjancenko O, Thomsen MC, Voldby Larsen M, Ussery DP (2013) PanFunPro: PAN-genome analysis based on FUNctional PROfiles. F1000Res 2:1–19

39.

Kayansamruaj P, Pirarat N, Kondo H, Hirono I, Rodkhum C (2015) Genomic comparison between pathogenic Streptococcus agalactiae isolated from Nile tilapia in Thailand and fish-derived ST7 strains. Infect Genet Evol 36:307–314. doi:10.1016/j.meegid.2015.10.009 PubMedCrossRef

40.

Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20(2):265–272. doi:10.1101/gr.097261.109 PubMedPubMedCentralCrossRef

41.

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. doi:10.1089/cmb.2012.0021 PubMedPubMedCentralCrossRef

42.

Rasmussen LH, Dargis R, Christensen JJ, Skovgaard O, Nielsen XC (2016) Draft genome sequence of type strain streptococcus gordonii ATCC 10558. Genome Announc 4(1). doi:10.1128/genomeA.01745-15

43.

Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75. doi:10.1186/1471-2164-9-75

44.

Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acid Res 42(Database issue):D206–D214. doi:10.1093/nar/gkt1226

45.

Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. doi:10.1093/nar/gkh340 PubMedPubMedCentralCrossRef

46.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. doi:10.1093/molbev/mst197 PubMedPubMedCentralCrossRef

47.

Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O (2014) Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One 9(8):e104984. doi:10.1371/journal.pone.0104984

48.

Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42(Database issue):D222–D230. doi:10.1093/nar/gkt1223 PubMedCrossRef

49.

Haft DH, Selengut JD, White O (2003) The TIGRFAMs database of protein families. Nucleic Acids Res 31(1):371–373PubMedPubMedCentralCrossRef

50.

Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C, Madera M, Chothia C, Gough J (2009) SUPERFAMILY–sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res 37(Database issue):D380–D386. doi:10.1093/nar/gkn762 PubMedCrossRef

51.

Zdobnov EM, Apweiler R (2001) InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17(9):847–848PubMedCrossRef

52.

Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659. doi:10.1093/bioinformatics/btl158 PubMedCrossRef

53.

Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28(23):3150–3152. doi:10.1093/bioinformatics/bts565 PubMedPubMedCentralCrossRef

54.

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704PubMedCrossRef

55.

Kiratisin P, Li L, Murray PR, Fischer SH (2005) Use of housekeeping gene sequencing for species identification of viridans streptococci. Diagn Microbiol Infect Dis 51(4):297–301. doi:10.1016/j.diagmicrobio.2004.12.001 PubMedCrossRef

56.

Kawamura Y, Whiley RA, Shu SE, Ezaki T, Hardie JM (1999) Genetic approaches to the identification of the mitis group within the genus Streptococcus. Microbiology 145(Pt 9):2605–2613. doi:10.1099/00221287-145-9-2605 PubMedCrossRef

57.

57. Wuyts V, Denayer S, Roosens NH, Mattheus W, Bertrand S, Marchal K, Dierick K, De Keersmaecker SC (2015) Whole genome sequence analysis of salmonella enteritidis PT4 outbreaks from a national reference laboratory’s viewpoint. PLoS Curr 7. doi:10.1371/currents.outbreaks.aa5372d90826e6cb0136ff66bb7a62fc

58.

Gao XY, Zhi XY, Li HW, Klenk HP, Li WJ (2014) Comparative genomics of the bacterial genus Streptococcus illuminates evolutionary implications of species groups. PLoS One 9(6):e101229. doi:10.1371/journal.pone.0101229

59.

Lefebure T, Stanhope MJ (2007) Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8(5):R71. doi:10.1186/gb-2007-8-5-r71 PubMedPubMedCentralCrossRef

60.

Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13(9):2178–2189. doi:10.1101/gr.1224503 PubMedPubMedCentralCrossRef

61.

Enright AJ, Van Dongen S, Ouzounis CA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30(7):1575–1584PubMedPubMedCentralCrossRef

Title: Whole genome sequencing as a tool for phylogenetic analysis of clinical strains of Mitis group streptococci
Authors: L. H. Rasmussen
R. Dargis
K. Højholt
J. J. Christensen
O. Skovgaard
U. S. Justesen
F. S. Rosenvinge
C. Moser
O. Lukjancenko
S. Rasmussen
X. C. Nielsen
Publication date: 01-10-2016
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Clinical Microbiology & Infectious Diseases / Issue 10/2016
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI: https://doi.org/10.1007/s10096-016-2700-2

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