A global map of genetic diversity in Babesia microti reveals strong population structure and identifies variants associated with clinical relapse

Nature Microbiology

Volumn 1, Issue 7, 2016, Pages

  Lemieux, Jacob E ^a,b   Tran, Alice D ^c   Freimark, Lisa ^a   Schaffner, Stephen F ^a   Goethert, Heidi ^d   Andersen, Kristian G ^a,e   Bazner, Suzane ^b   Li, Amy ^a   McGrath, Graham ^b   Sloan, Lynne ^f   Vannier, Edouard ^g   Milner, Dan ^h   Pritt, Bobbi ^f   Rosenberg, Eric ^b   Telford, Sam ^d   Bailey, Jeffrey A ^c   Sabeti, Pardis C ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d TUFTS UNIVERSITY   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f MAYO CLINIC   (United States)

^g TUFTS MEDICAL CENTER   (United States)

^h BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATOVAQUONE; AZITHROMYCIN; CYTOCHROME B; PROTEIN BINDING; RIBOSOMAL PROTEIN L4; RIBOSOME PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL; BABESIA MICROTI; GENETIC VARIATION; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; HUMAN; METABOLISM; PARASITOLOGY; PIROPLASMOSIS; RECURRENT DISEASE; UNITED STATES; ZOONOSIS;

AMINO ACID SUBSTITUTION; ANIMALS; ATOVAQUONE; AZITHROMYCIN; BABESIA MICROTI; BABESIOSIS; CYTOCHROMES B; GENETIC VARIATION; GENOME, PROTOZOAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; PROTEIN BINDING; RECURRENCE; RIBOSOMAL PROTEINS; UNITED STATES; ZOONOSES;

EID: 84991294494     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.79     Document Type: Article

References (50)

1. Vannier, E. & Krause, P. J. Human babesiosis. N. Engl. J. Med. 366, 2397-2407 (2012).
2. Ruebush, T. K. & Spielman, A. Human babesiosis in the United States. Ann. Intern. Med. 88, 263-263 (1978).
3. Krause, P. J. et al. Persistent and relapsing babesiosis in immunocompromised patients. Clin. Infect. Dis. 46, 370-376 (2008).
4. Vyas, J. M., Telford, S. R. & Robbins, G. K. Treatment of refractory Babesia microti infection with atovaquone-proguanil in an HIV-infected patient: case report. Clin. Infect. Dis. 45, 1588-1590 (2007).
5. Wormser, G. P. et al. Emergence of resistance to azithromycin-atovaquone in immunocompromised patients with Babesia microti infection. Clin. Infect. Dis. 50, 381-386 (2010).
6. Telford, S. R., III. Babesial infections in humans and wildlife. Parasitic Protozoa 5, 1-47 (1993).
7. Herwaldt, B. L. et al. Transfusion-associated babesiosis in the United States: a description of cases. Ann. Intern. Med. 155, 509-519 (2011).
8. Yager, P. H., Luginbuhl, L. M. & Dekker, J. P. Case 6-2014. N. Engl. J. Med. 370, 753-762 (2014).
9. Clark, I. A. & Jacobson, L. S. Do babesiosis and malaria share a common disease process. Ann. Trop. Med. Parasitol. 92, 483-488 (1998).
10. Hatcher, J. C., Greenberg, P. D., Antique, J. & Jimenez-Lucho, V. E. Severe babesiosis in Long Island: review of 34 cases and their complications. Clin. Infect. Dis. 32, 1117-1125 (2001).
11. Meldrum, S. C., Birkhead, G. S., White, D. J., Benach, J. L. & Morse, D. L. Human babesiosis in New York state: an epidemiological description of 136 cases. Clin. Infect. Dis. 15, 1019-1023 (1992).
12. Menis, M. et al. Babesiosis occurrence among the elderly in the United States, as recorded in large Medicare databases during 2006-2013. PLoS ONE 10, e0140332 (2015).
13. Hildebrandt, A. et al. First confirmed autochthonous case of human Babesia microti infection in Europe. Eur. J. Clin. Microbiol. Infect. Dis. 26, 595-601 (2007).
14. Wei, Q. et al. Human babesiosis in Japan: isolation of Babesia microti-like parasites from an asymptomatic transfusion donor and from a rodent from an area where babesiosis is endemic. J. Clin. Microbiol. 39, 2178-2183 (2001).
15. Senanayake, S. N. et al. First report of human babesiosis in Australia. Med. J. Aust. 196, 350-352 (2012).
16. Western, K. A., Benson, G. D., Gleason, N. N., Healy, G. R. & Schultz, M. G. Babesiosis in a Massachusetts resident. N. Engl. J. Med. 283, 854-856 (1970).
17. Centers for Disease Control and Prevention (CDC). Babesiosis surveillance-18 states, 2011. Morb. Mortal. Wkly Rep. 61, 505-509 (2012).
18. Krause, P. J. et al. Increasing health burden of human babesiosis in endemic sites. Am. J. Trop. Med. Hyg. 68, 431-436 (2003).
19. Stafford, K. C.III et al. Expansion of zoonotic babesiosis and reported human cases, Connecticut, 2001-2010. J. Med. Entomol. 51, 245-252 (2014).
20. Goethert, H. K. & Telford, S. R. Not 'out of Nantucket': Babesia microti in southern New England comprises at least two major populations. Parasites Vectors 7, 546 (2014).
21. Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).
22. Homer, M. J. et al. A polymorphic multigene family encoding an immunodominant protein from Babesia microti. J. Clin. Microbiol. 38, 362-368 (2000).
23. Srivastava, I. K., Morrisey, J. M., Darrouzet, E., Daldal, F. & Vaidya, A. B. Resistance mutations reveal the atovaquone-binding domain of cytochrome b in malaria parasites. Mol. Microbiol. 33, 704-711 (1999).
24. Korsinczky, M. et al. Mutations in Plasmodium falciparum cytochrome b that are associated with atovaquone resistance are located at a putative drug-binding site. Antimicrob. Agents Chemother. 44, 2100-2108 (2000).
25. Matsuu, A., Miyamoto, K., Ikadai, H., Okano, S. & Higuchi, S. Short report: cloning of the Babesia gibsoni cytochrome b gene and isolation of three single nucleotide polymorphisms from parasites present after atovaquone treatment. Am. J. Trop. Med. Hyg. 74, 593-597 (2006).
26. Sidhu, A. B. S. et al. In vitro efficacy, resistance selection, and structural modeling studies implicate the malarial parasite apicoplast as the target of azithromycin. J. Biol. Chem. 282, 2494-2504 (2007).
27. Malbruny, B. et al. Resistance to macrolides in clinical isolates of Streptococcus pyogenes due to ribosomal mutations. J. Antimicrob. Chemother. 49, 935-939 (2002).
28. Chittum, H. S. & Champney, W. S. Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli. J. Bacteriol. 176, 6192-6198 (1994).
29. McFadden, D. C., Tomavo, S., Berry, E. A. & Boothroyd, J. C. Characterization of cytochrome b from Toxoplasma gondii and Q(o) domain mutations as a mechanism of atovaquone-resistance. Mol. Biochem. Parasitol. 108, 1-12 (2000).
30. Pihlajamäki, M. et al. Ribosomal mutations in Streptococcus pneumoniae clinical isolates. Antimicrob. Agents Chemother. 46, 654-658 (2002).
31. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010).
32. McKenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
33. Pages, H., Aboyoun, P., Gentleman, R. & Deb Roy, S. Biostrings (Bioconductor); http://bioconductor.fhcrc.org/packages/release/bioc/html/Biostrings.html
34. Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
35. Pfeifer, B., Wittelsbürger, U., Onsins, S. E. R. & Lercher, M. J. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol. Biol. Evol. 31, 1929-1936 (2014).
36. South, A. rworldmap: a new R package for mapping global data. The R Journal 3, 35-43 (2011).
37. Charif, D. & Lobry, J. R. in Structural Approaches to Sequence Evolution 207-232 (Springer, 2007).
38. Rutherford, K. et al. Artemis: sequence visualization and annotation. Bioinformatics 16, 944-945 (2000).
39. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
40. Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).
41. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).
42. Cornillot, E. et al. Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Res. 40, 9102-9114 (2012).
43. Nei, M. & Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418-426 (1986).
44. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300 (1995).
45. Birth, D., Kao, W.-C. & Hunte, C. Structural analysis of atovaquone-inhibited cytochrome bc1 complex reveals the molecular basis of antimalarial drug action. Nature Commun. 5, 4029 (2014).
46. Bulkley, D., Innis, C. A., Blaha, G. & Steitz, T. A. Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc. Natl Acad. Sci. USA 107, 17158-17163 (2010).
47. Simpson, J. T. et al. ABySS: a parallel assembler for short read sequence data. Genome Res. 19, 1117-1123 (2009).
48. Delcher, A. L. et al. Alignment of whole genomes. Nucleic Acids Res. 27, 2369-2376 (1999).
49. Melnikov, A. et al. Hybrid selection for sequencing pathogen genomes from clinical samples. Genome Biol. 12, R73 (2011).
50. Gnirke, A. et al. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nature Biotechnol. 27, 182-189 (2009).