Comprehensive phylogenetic analysis of bovine non-aureus staphylococci species based on whole-genome sequencing

Frontiers in Microbiology

Volumn 7, Issue DEC, 2016, Pages

  Naushad, Sohail ^a,b   Barkema, Herman W ^a,b   Luby, Christopher ^b,c   Condas, Larissa A Z ^a,b   Nobrega, Diego B ^a,b   Carson, Domonique A ^a,b   De Buck, Jeroen ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b Canadian Bovine Mastitis and Milk Quality Research Network   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Bovine intramammary infection; Coagulase negative staphylococci; Non aureus staphylococci; Phylogenetic trees; Whole genome sequencing

Indexed keywords

RNA 16S;

ANTIBIOTIC RESISTANCE; ARTICLE; CELL DIVISION; DNA EXTRACTION; GENE; HOST RANGE; HSP60 GENE; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; RPOB GENE; SODA GENE; STAPHYLOCOCCUS; TUF GENE; VIRULENCE; WHOLE GENOME SEQUENCING;

EID: 85008967215     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01990     Document Type: Article

References (75)

1. Aarestrup, F. M., Wegener, H. C., Rosdahl, V. T., and Jensen, N. E. (1995). Staphylococcal and other bacterial species associated with intramammary infections in Danish dairy herds. Acta Vet. Scand. 36, 475-487.
2. Beiko, R. G., Harlow, T. J., and Ragan, M. A. (2005). Highways of gene sharing in prokaryotes. Proc. Natl. Acad. Sci. U.S.A. 102, 14332-14337. doi: 10.1073/pnas.0504068102
3. Bernard, G., Chan, C. X., and Ragan, M. A. (2016). Alignment-free microbial phylogenomics under scenarios of sequence divergence, genome rearrangement and lateral genetic transfer. Sci. Rep. 6:28970. doi: 10.1038/srep28970
4. Boc, A., Diallo, A. B., and Makarenkov, V. (2012). T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40, W573-W579. doi: 10.1093/nar/gks485
5. Burbrink, F. T., and Pyron, R. A. (2011). The impact of gene-tree/species-tree discordance on diversification-rate estimation. Evolution 65, 1851-1861. doi: 10.1111/j.1558-5646.2011.01260.x
6. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., et al. (2009). BLAST+: architecture and applications. BMC Bioinform. 10:421. doi: 10.1186/1471-2105-10-421
7. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552. doi: 10.1093/oxfordjournals.molbev.a026334
8. Chung, Y., and Ané, C. (2011). Comparing two Bayesian methods for gene tree/species tree reconstruction: simulations with incomplete lineage sorting and horizontal gene transfer. Syst. Biol. 60, 261-275. doi: 10.1093/sysbio/syr003
9. Degnan, J. H., and Rosenberg, N. A. (2006). Discordance of species trees with their most likely gene trees. PLoS Genet. 2:e68. doi: 10.1371/journal.pgen.0020068
10. De Vliegher, S., Fox, L. K., Piepers, S., McDougall, S., and Barkema, H. W. (2012). Invited review: mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J. Dairy Sci. 95, 1025-1040. doi: 10.3168/jds.2010-4074
11. De Vliegher, S., Opsomer, G., Vanrolleghem, A., Devriese, L. A., Sampimon, O. C., Sol, J., et al. (2004). In vitro growth inhibition of major mastitis pathogens by Staphylococcus chromogenes originating from teat apices of dairy heifers. Vet. Microbiol. 101, 215-221. doi: 10.1016/j.vetmic.2004.03.020
12. Dos Santos, D. C., Lange, C. C., Avellar-Costa, P., Dos Santos, K. R., Brito, M. A., and Giambiagi-deMarval, M. (2016). Staphylococcus chromogenes, a coagulase-negative staphylococcus species that can clot plasma. J. Clin. Microbiol. 54, 1372-1375. doi: 10.1128/JCM.03139-15
13. Drancourt, M., and Raoult, D. (2002). rpoB gene sequence-based Identification of Staphylococcus species. J. Clin. Microbiol. 40, 1333-1338. doi: 10.1128/JCM.40.4.1333-1338.2002
14. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340
15. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
16. Frey, Y., Rodriguez, J. P., Thomann, A., Schwendener, S., and Perreten, V. (2013). Genetic characterization of antimicrobial resistance in coagulase-negative staphylococci from bovine mastitis milk. J. Dairy Sci. 96, 2247-2257. doi: 10.3168/jds.2012-6091
17. Ghebremedhin, B., Layer, F., König, W., and König, B. (2008). Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J. Clin. Microbiol. 46, 1019-1025. doi: 10.1128/JCM.02058-07
18. Gillespie, B. E., Headrick, S. I., Boonyayatra, S., and Oliver, S. P. (2009). Prevalence and persistence of coagulase-negative Staphylococcus species in three dairy research herds. Vet. Microbiol. 134, 65-72. doi: 10.1016/j.vetmic.2008.09.007
19. Gurevich, A., Saveliev, V., Vyahhi, N., and Tesler, G. (2013). QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072-1075. doi: 10.1093/bioinformatics/btt086
20. Honkanen-Buzalski, T., Myllys, V., and Pyörölö, S. (1994). Bovine clinical mastitis due to coagulase-negative staphylococci and their susceptibility to antimicrobials. Zentralbl. Veterinarmed. B 41, 344-350. doi: 10.1111/j.1439-0450.1994.tb00237.x
21. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Compu. Appl. Biosci. 8, 275-282. doi: 10.1093/bioinformatics/8.3.275
22. Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010
23. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. doi: 10.1007/BF01731581
24. Kloos, W. E., Ballard, D. N., George, C. G., Webster, J. A., Hubner, R. J., Ludwig, W., et al. (1998a). Delimiting the genus Staphylococcus through description of Macrococcus caseolyticus gen. nov., comb. nov. and Macrococcus equipercicus sp. nov., and Macrococcus bovicus sp. no. and Macrococcus carouselicus sp. nov. Int. J. Syst. Bacteriol. 48(Pt 3), 859-877. doi: 10.1099/00207713-48-3-859
25. Kloos, W. E., George, C. G., Olgiate, J. S., Van Pelt, L., McKinnon, M. L., Zimmer, B. L., et al. (1998b). Staphylococcus hominis subsp. novobiosepticus subsp. nov., a novel trehalose-and N-acetyl-D-glucosamine-negative, novobiocin-and multiple-antibiotic-resistant subspecies isolated from human blood cultures. Int. J. Syst. Bacteriol. 48(Pt 3), 799-812. doi: 10.1099/00207713-48-3-799
26. Köster, J., and Rahmann, S. (2012). Snakemake-a scalable bioinformatics workflow engine. Bioinformatics 28, 2520-2522. doi: 10.1093/bioinformatics/bts480
27. Kupczok, A., Schmidt, H. A., and von Haeseler, A. (2010). Accuracy of phylogeny reconstruction methods combining overlapping gene data sets. Algorithms Mol. Biol. 5:37. doi: 10.1186/1748-7188-5-37
28. Kwok, A. Y. Chow A W. (2003). Phylogenetic study of Staphylococcus and Macrococcus species based on partial hsp60 gene sequences. Int. J. Syst. Evol. Microbiol. 53, 87-92. doi: 10.1099/ijs.0.02210-0
29. Laevens, H., Deluyker, H., Schukken, Y. H., De Meulemeester, L., Vandermeersch, R., De Muêlenaere, E., et al. (1997). Influence of parity and stage of lactation on the somatic cell count in bacteriologically negative dairy cows. J. Dairy Sci. 80, 3219-3226. doi: 10.3168/jds.S0022-0302(97)76295-7
30. Lamers, R. P., Muthukrishnan, G., Castoe, T. A., Tafur, S., Cole, A. M., and Parkinson, C. L. (2012). Phylogenetic relationships among Staphylococcus species and refinement of cluster groups based on multilocus data. BMC Evol. Biol. 12:171. doi: 10.1186/1471-2148-12-171
31. Li, H., and Durbin, R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595. doi: 10.1093/bioinformatics/btp698
32. Maddison, W. P., and Knowles, L. L. (2006). Inferring phylogeny despite incomplete lineage sorting. Syst. Biol. 55, 21-30. doi: 10.1080/10635150500354928
33. Makarenkov, V., and Leclerc, B. (2000). Comparison of additive trees using circular orders. J. Comput. Biol. 7, 731-744. doi: 10.1089/106652701446170
34. Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10-12. doi: 10.14806/ej.17.1.200
35. Matthews, K. R., Harmon, R. J., and Smith, B. A. (1990). Protective effect of Staphylococcus chromogenes infection against Staphylococcus aureus infection in the lactating bovine mammary gland. J. Dairy Sci. 73, 3457-3462. doi: 10.3168/jds.S0022-0302(90)79044-3
36. Mellmann, A., Becker, K., von Eiff, C., Keckevoet, U., Schumann, P., and Harmsen, D. (2006). Sequencing and staphylococci identification. Emer. Infect. Dis. 12, 333-336. doi: 10.3201/eid1202.050962
37. Mendes, F. K., and Hahn, M. W. (2016). Gene tree discordance causes apparent substitution rate variation. Syst. Biol. 65, 711-721. doi: 10.1093/sysbio/syw018
38. Naushad, S., Adeolu, M., Goel, N., Khadka, B., Al-Dahwi, A., and Gupta, R. S. (2015a). Phylogenomic and molecular demarcation of the core members of the polyphyletic Pasteurellaceae genera Actinobacillus, Haemophilus, and Pasteurella. Int. J. Genomics 2015:198560. doi: 10.1155/2015/198560
39. Naushad, S., Adeolu, M., Wong, S., Sohail, M., Schellhorn, H. E., and Gupta, R. S. (2015b). A phylogenomic and molecular marker based taxonomic framework for the order Xanthomonadales: proposal to transfer the families Algiphilaceae and Solimonadaceae to the order Nevskiales ord. nov. and to create a new family within the order Xanthomonadales, the family Rhodanobacteraceae fam. nov., containing the genus Rhodanobacter and its closest relatives. Antonie Van Leeuwenhoek 107, 467-485. doi: 10.1007/s10482-014-0344-8
40. Nei, M., and Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford: Oxford University Press.
41. Nurk, S., Bankevich, A., Antipov, D., Gurevich, A. A., Korobeynikov, A., Lapidus, A., et al. (2013). Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J. Comput. Biol. 20, 714-737. doi: 10.1089/cmb.2013.0084
42. Otto, M. (2013). Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence. Bioessays 35, 4-11. doi: 10.1002/bies.201200112
43. Piepers, S., De Meulemeester, L., de Kruif, A., Opsomer, G., Barkema, H. W., and De Vliegher, S. (2007). Prevalence and distribution of mastitis pathogens in subclinically infected dairy cows in Flanders, Belgium. J. Dairy Res. 74, 478-483. doi: 10.1017/S0022029907002841
44. Piepers, S., De Vliegher, S., de Kruif, A., Opsomer, G., and Barkema, H. W. (2009). Impact of intramammary infections in dairy heifers on future udder health, milk production, and culling. Vet. Microbiol. 134, 113-120. doi: 10.1016/j.vetmic.2008.09.017
45. Piessens, V., Van Coillie, E., Verbist, B., Supré, K., Braem, G., Van Nuffel, A., et al. (2011). Distribution of coagulase-negative Staphylococcus species from milk and environment of dairy cows differs between herds. J. Dairy Sci. 94, 2933-2944. doi: 10.3168/jds.2010-3956
46. Price, M. N., Dehal, P. S., and Arkin, A. P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi: 10.1371/journal.pone.0009490
47. Puigbò, P., Wolf, Y. I., and Koonin, E. V. (2010). The tree and net components of prokaryote evolution. Genome Biol. Evol. 2, 745-756. doi: 10.1093/gbe/evq062
48. Pyörälä, S., and Taponen, S. (2009). Coagulase-negative staphylococci-Emerging mastitis pathogens. Vet. Microbiol. 134, 3-8. doi: 10.1016/j.vetmic.2008.09.015
49. Quinlan, A. R., and Hall, I. M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842. doi: 10.1093/bioinformatics/btq033
50. Rajala-Schultz, P. J., Torres, A. H., Degraves, F. J., Gebreyes, W. A., and Patchanee, P. (2009). Antimicrobial resistance and genotypic characterization of coagulase-negative staphylococci over the dry period. Vet. Microbiol. 134, 55-64. doi: 10.1016/j.vetmic.2008.09.008
51. Reyher, K. K., Dufour, S., Barkema, H. W., Des Coteaux, L., Devries, T. J., Dohoo, I. R., et al. (2011). The National Cohort of Dairy Farms-a data collection platform for mastitis research in Canada. J. Dairy Sci. 94, 1616-1626. doi: 10.3168/jds.2010-3180
52. Robinson, D. F., and Foulds, L. R. (1981). Comparison of phylogenetic trees. Math. Biosci. 53, 131-147. doi: 10.1016/0025-5564(81)90043-2
53. Rokas, A., Williams, B. L., King, N., and Carroll, S. B. (2003). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798-804. doi: 10.1038/nature02053
54. Sampimon, O. C., Barkema, H. W., Berends, I. M. G. A., Sol, J., and Lam, T. J. G. M. (2009). Prevalence and herd-level risk factors for intramammary infection with coagulase-negative staphylococci in Dutch dairy herds. Vet. Microbiol. 134, 37-44. doi: 10.1016/j.vetmic.2008.09.010
55. Schukken, Y. H., González, R. N., Tikofsky, L. L., Schulte, H. F., Santisteban, C. G., Welcome, F. L., et al. (2009). CNS mastitis: nothing to worry about? Vet. Microbiol. 134, 9-14. doi: 10.1016/j.vetmic.2008.09.014
56. Seemann, T. (2014). Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068-2069. doi: 10.1093/bioinformatics/btu153
57. Segata, N., Börnigen, D., Morgan, X. C., and Huttenhower, C. (2013). PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat. Commun. 4, 2304. doi: 10.1038/ncomms3304
58. Shah, M. M., Iihara, H., Noda, M., Song, S. X., Nhung, P. H., Ohkusu, K., et al. (2007). dnaJ gene sequence-based assay for species identification and phylogenetic grouping in the genus Staphylococcus. Int. J. Syst. Evol. Microbiol. 57, 25-30. doi: 10.1099/ijs.0.64205-0
59. Stadler, T., Degnan, J. H., and Rosenberg, N. A. (2016). Does gene tree discordance explain the mismatch between macroevolutionary models and empirical patterns of tree shape and branching times? Syst. Biol. 65, 628-639. doi: 10.1093/sysbio/syw019
60. Supré, K., Haesebrouck, F., Zadoks, R. N., Vaneechoutte, M., Piepers, S., and De Vliegher, S. (2011). Some coagulase-negative Staphylococcus species affect udder health more than others. J. Dairy Sci. 94, 2329-2340. doi: 10.3168/jds.2010-3741
61. Svec, P., Vancanneyt, M., Sedlácek, I., Engelbeen, K., Stetina, V., Swings, J., et al. (2004). Reclassification of Staphylococcus pulvereri Zakrzewska-Czerwinska et al. 1995 as a later synonym of Staphylococcus vitulinus Webster et al. 1994. Int. J. Syst. Evol. Microbiol. 54, 2213-2215. doi: 10.1099/ijs.0.63080-0
62. Takahashi, T., Satoh, I., and Kikuchi, N. (1999). Phylogenetic relationships of 38 taxa of the genus Staphylococcus based on 16S rRNA gene sequence analysis. Int. J. Syst. Bacteriol. 49(Pt 2), 725-728. doi: 10.1099/00207713-49-2-725
63. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
64. Taponen, S., Koort, J., Björkroth, J., Saloniemi, H., and Pyörälä, S. (2007). Bovine intramammary infections caused by coagulase-negative staphylococci may persist throughout lactation according to amplified fragment length polymorphism-based analysis. J. Dairy Sci. 90, 3301-3307. doi: 10.3168/jds.2006-860
65. Taponen, S., Nykäsenoja, S., Pohjanvirta, T., Pitkälä, A., and Pyörälä, S. (2015). Species distribution and in vitro antimicrobial susceptibility of coagulase-negative staphylococci isolated from bovine mastitic milk. Acta Vet. Scand. 58, 12. doi: 10.1186/s13028-016-0193-8
66. Taponen, S., and Pyörälä, S. (2009). Coagulase-negative staphylococci as cause of bovine mastitis-Not so different from Staphylococcus aureus? Vet. Microbiol. 134, 29-36. doi: 10.1016/j.vetmic.2008.09.011
67. Taponen, S., Supré, K., Piessens, V., Van Coillie, E., De Vliegher, S., and Koort, J. M. (2012). Staphylococcus agnetis sp. nov., a coagulase-variable species from bovine subclinical and mild clinical mastitis. Int. J. Syst. Evol. Microbiol. 62, 61-65. doi: 10.1099/ijs.0.028365-0
68. Thorberg, B. M., Danielsson-Tham, M. L., Emanuelson, U., and Persson Waller, K. (2009). Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J. Dairy Sci. 92, 4962-4970. doi: 10.3168/jds.2009-2184
69. Vanderhaeghen, W., Piepers, S., Leroy, F., Van Coillie, E., Haesebrouck, F., and De Vliegher, S. (2014). Invited review: effect, persistence, and virulence of coagulase-negative Staphylococcus species associated with ruminant udder health. J. Dairy Sci. 97, 5275-5293. doi: 10.3168/jds.2013-7775
70. Vanderhaeghen, W., Piepers, S., Leroy, F., Van Coillie, E., Haesebrouck, F., and De Vliegher, S. (2015). Identification, typing, ecology and epidemiology of coagulase negative staphylococci associated with ruminants. Vet. J. 203, 44-51. doi: 10.1016/j.tvjl.2014.11.001
71. Whelan, S., and Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699. doi: 10.1093/oxfordjournals.molbev.a003851
72. Woodward, W. D., Besser, T. E., Ward, A. C., and Corbeil, L. B. (1987). In vitro growth inhibition of mastitis pathogens by bovine teat skin normal flora. Can. J. Vet. Res. 51, 27-31.
73. Woodward, W. D., Ward, A. C. S., Fox, L. K., and Corbeil, L. B. (1988). Teat skin normal flora and colonization with mastitis pathogen inhibitors. Vet. Microbiol. 17, 357-365. doi: 10.1016/0378-1135(88)90049-1
74. Wu, D., Hugenholtz, P., Mavromatis, K., Pukall, R., Dalin, E., Ivanova, N. N., et al. (2009). A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056-1060. doi: 10.1038/nature08656
75. Zhang, Y.-Q., Ren, S.-X., Li, H.-L., Wang, Y.-X., Fu, G., Yang, J., et al. (2003). Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49, 1577-1593. doi: 10.1046/j.1365-2958.2003.03671.x