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Advances and challenges in barcoding pathogenic and environmental Leptospira

Published online by Cambridge University Press:  18 July 2017

VANINA GUERNIER ,
KATHRYN J. ALLAN  and
CYRILLE GOARANT Open the ORCID record for CYRILLE GOARANT [Opens in a new window]
VANINA GUERNIER
Affiliation:
Australian Institute of Tropical Health and Medicine, James Cook University, 1 James Cook Drive, Townsville, QLD 4811, Australia
KATHRYN J. ALLAN
Affiliation:
Institute of Biodiversity Animal Health and Comparative Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, University Avenue, Glasgow, G12 8QQ, UK
CYRILLE GOARANT*
Affiliation:
Institut Pasteur in New Caledonia, Institut Pasteur International Network, Leptospirosis Research and Expertise Unit, Noumea, New Caledonia. 11 rue Paul Doumer, BP 61; 98845 Noumea cedex, New Caledonia
*
*Corresponding author: Institut Pasteur in New Caledonia, Institut Pasteur International Network, Leptospirosis Research and Expertise Unit, Noumea, New Caledonia. 11 rue Paul Doumer, BP 61; 98845 Noumea cedex, New Caledonia. E-mail: [email protected]
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Summary

Leptospirosis is a zoonotic bacterial disease of global importance. A large spectrum of asymptomatic animal hosts can carry the infection and contribute to the burden of human disease. Environmental sources of human contamination also point to the importance of a hydrotelluric reservoir. Leptospirosis can be caused by as many as 15 different pathogenic or intermediate Leptospira species. However, classification of these bacteria remains complicated through the use of both serological and genetic classification systems that show poor correlation. With the advent of molecular techniques, DNA-based barcoding offers a conceptual framework that can be used for leptospirosis surveillance as well as source tracking. In this review, we summarize some of the current techniques, highlight significant successes and weaknesses and point to the future opportunities and challenges to successfully establish a widely applicable barcoding scheme for Leptospira.

Keywords

Leptospiraepidemiologyzoonotic reservoirbarcodinggenotyping
Type
Special Issue Review
Information
Parasitology , Volume 145 , Special Issue 5: Advances and challenges in barcoding of microbes, parasites, and their vectors and reservoirs , April 2018 , pp. 595 - 607
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Adler, B. (2015). History of leptospirosis and Leptospira. In Leptospira and Leptospirosis (ed. Adler, B.), vol. 387, pp. 1–9. Springer-Verlag, Heidelberg, Germany.CrossRefGoogle ScholarPubMed
Adler, B., Lo, M., Seemann, T. and Murray, G. L. (2011). Pathogenesis of leptospirosis: the influence of genomics. Veterinary Microbiology 153, 73–81.CrossRefGoogle ScholarPubMed
Agampodi, S. B., Peacock, S. J., Thevanesam, V., Nugegoda, D. B., Smythe, L., Thaipadungpanit, J., Craig, S. B., Burns, M. A., Dohnt, M., Boonsilp, S., Senaratne, T., Kumara, A., Palihawadana, P., Perera, S. and Vinetz, J. M. (2011). Leptospirosis outbreak in Sri Lanka in 2008: lessons for assessing the Global burden of disease. American Journal of Tropical Medicine and Hygiene 85, 471–478.CrossRefGoogle ScholarPubMed
Agampodi, S. B., Moreno, A. C., Vinetz, J. M. and Matthias, M. A. (2013). Utility and limitations of direct multi-locus sequence typing on qPCR-positive blood to determine infecting Leptospira strain. American Journal of Tropical Medicine and Hygiene 88, 184–185.CrossRefGoogle ScholarPubMed
Agampodi, S. B., Dahanayaka, N. J., Bandaranayaka, A. K., Perera, M., Priyankara, S., Weerawansa, P., Matthias, M. A. and Vinetz, J. M. (2014). Regional differences of leptospirosis in Sri Lanka: observations from a flood-associated outbreak in 2011. PLoS Neglected Tropical Diseases 8, e2626.CrossRefGoogle ScholarPubMed
Ahmed, A., Engelberts, M. F., Boer, K. R., Ahmed, N. and Hartskeerl, R. A. (2009). Development and validation of a real-time PCR for detection of pathogenic Leptospira species in clinical materials. PLoS ONE 4, e7093.CrossRefGoogle ScholarPubMed
Ahmed, A., Grobusch, M. P., Klatser, P. R. and Hartskeerl, R. A. (2012). Molecular approaches in the detection and characterization of Leptospira. Journal of Bacteriology and Parasitology 3, 1000133.Google Scholar
Ahmed, N., Devi, S. M., Valverde Mde, L., Vijayachari, P., Machang'u, R. S., Ellis, W. A. and Hartskeerl, R. A. (2006). Multilocus sequence typing method for identification and genotypic classification of pathogenic Leptospira species. Annals of Clinical Microbiology and Antimicrobials 5, 28.CrossRefGoogle ScholarPubMed
Allan, K. J. (2016). Leptospirosis in northern Tanzania: investigating the role of rodents and ruminant livestock in a neglected public health problem. In Institute of Biodiversity, Animal Health and Comparative Medicine 298 PhD Glasgow, Scotland, UK, University of Glasgow. http://theses.gla.ac.uk/7565/Google Scholar
Allan, K. J., Biggs, H. M., Halliday, J. E., Kazwala, R. R., Maro, V. P., Cleaveland, S. and Crump, J. A. (2015). Epidemiology of leptospirosis in Africa: a systematic review of a neglected zoonosis and a paradigm for ‘one health’ in Africa. PLoS Neglected Tropical Diseases 9, e0003899.Google Scholar
Ayral, F., Djelouadji, Z., Raton, V., Zilber, A. L., Gasqui, P., Faure, E., Baurier, F., Vourc'h, G., Kodjo, A. and Combes, B. (2016). Hedgehogs and mustelid species: major carriers of pathogenic Leptospira, a survey in 28 animal species in France (20122015). PLoS ONE 11, e0162549.Google Scholar
Baker, C. C., Bittleston, L. S., Sanders, J. G. and Pierce, N. E. (2016). Dissecting host-associated communities with DNA barcodes. Philos Trans R Soc Lond B Biol Sci, 371, 1702. pii: 20150328. doi: 10.1098/rstb.2015.0328.CrossRefGoogle ScholarPubMed
Balamurugan, V., Gangadhar, N. L., Mohandoss, N., Thirumalesh, S. R., Dhar, M., Shome, R., Krishnamoorthy, P., Prabhudas, K. and Rahman, H. (2013). Characterization of Leptospira isolates from animals and humans: phylogenetic analysis identifies the prevalence of intermediate species in India. Springerplus 2, 362.Google Scholar
Bezerra da Silva, J., Carvalho, E., Hartskeerl, R. A. and Ho, P. L. (2011). Evaluation of the use of selective PCR amplification of LPS biosynthesis genes for molecular typing of Leptospira at the serovar level. Current Microbiology 62, 518–524.CrossRefGoogle ScholarPubMed
Boonsilp, S., Thaipadungpanit, J., Amornchai, P., Wuthiekanun, V., Bailey, M. S., Holden, M. T., Zhang, C., Jiang, X., Koizumi, N., Taylor, K., Galloway, R., Hoffmaster, A. R., Craig, S., Smythe, L. D., Hartskeerl, R. A., Day, N. P., Chantratita, N., Feil, E. J., Aanensen, D. M., Spratt, B. G. and Peacock, S. J. (2013). A single multilocus sequence typing (MLST) scheme for seven pathogenic Leptospira species. PLoS Neglected Tropical Diseases 7, e1954.CrossRefGoogle ScholarPubMed
Bourhy, P., Bremont, S., Zinini, F., Giry, C. and Picardeau, M. (2011). Comparison of real-time PCR assays for the detection of pathogenic Leptospira spp. in blood and identification of variations in target sequences. Journal of Clinical Microbiology 49, 2154–2160.Google Scholar
Bourhy, P., Collet, L., Lernout, T., Zinini, F., Hartskeerl, R., van der Linden, H., Thiberge, J. M., Diancourt, L., Brisse, S., Giry, C., Pettinelli, F. and Picardeau, M. (2012). Human Leptospira isolates circulating in Mayotte (Indian Ocean) have unique serological and molecular features. Journal of Clinical Microbiology 50, 307–311.Google Scholar
Bourhy, P., Collet, L., Brisse, S. and Picardeau, M. (2014). Leptospira mayottensis sp. nov., a pathogenic Leptospira species isolated from humans. International Journal of Systematic and Evolutionary Microbiology 64, 4061–4067.Google Scholar
Bulach, D. M., Zuerner, R. L., Wilson, P., Seemann, T., McGrath, A., Cullen, P. A., Davis, J., Johnson, M., Kuczek, E., Alt, D. P., Peterson-Burch, B., Coppel, R. L., Rood, J. I., Davies, J. K. and Adler, B. (2006). Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proceedings of the National Academy of Sciences of the USA 103, 14560–14565.CrossRefGoogle ScholarPubMed
Cerqueira, G. M. and Picardeau, M. (2009). A century of Leptospira strain typing. Infection, Genetics and Evolution 9, 760–768.Google Scholar
Cerqueira, G. M., McBride, A. J., Hartskeerl, R. A., Ahmed, N., Dellagostin, O. A., Eslabao, M. R. and Nascimento, A. L. (2010). Bioinformatics describes novel loci for high resolution discrimination of Leptospira isolates. PLoS ONE 5, e15335.Google Scholar
Cosson, J. F., Picardeau, M., Mielcarek, M., Tatard, C., Chaval, Y., Suputtamongkol, Y., Buchy, P., Jittapalapong, S., Herbreteau, V. and Morand, S. (2014). Epidemiology of Leptospira transmitted by rodents in southeast Asia. PLoS Neglected Tropical Diseases 8, e2902.Google Scholar
Costa, F., Hagan, J. E., Calcagno, J., Kane, M., Torgerson, P., Martinez-Silveira, M. S., Stein, C., Abela-Ridder, B. and Ko, A. I. (2015). Global morbidity and mortality of leptospirosis: a systematic review. PLoS Neglected Tropical Diseases 9, e0003898.Google Scholar
Dietrich, M., Wilkinson, D. A., Soarimalala, V., Goodman, S. M., Dellagi, K. and Tortosa, P. (2014). Diversification of an emerging pathogen in a biodiversity hotspot: Leptospira in endemic small mammals of Madagascar. Molecular Ecology 23, 2783–2796.CrossRefGoogle Scholar
Dupuis, J. R., Roe, A. D. and Sperling, F. A. (2012). Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Molecular Ecology 21, 4422–4436.Google Scholar
Durack, J., Burke, T. P. and Portnoy, D. A. (2015). A prl mutation in SecY suppresses secretion and virulence defects of Listeria monocytogenes secA2 mutants. Journal of Bacteriology 197, 932–942.Google Scholar
Faine, S., Adler, B., Bolin, C. and Perolat, P. (1999). Leptospira and Leptospirosis, 2nd Edn, MedSci, Melbourne, Vic., Australia.Google Scholar
Fenner, J. S., Anjum, M. F., Randall, L. P., Pritchard, G. C., Wu, G., Errington, J., Dalley, C. G. and Woodward, M. J. (2010). Analysis of 16S rDNA sequences from pathogenic Leptospira serovars and use of single nucleotide polymorphisms for rapid speciation by D-HPLC. Research in Veterinary Science 89, 48–57.CrossRefGoogle ScholarPubMed
Fouts, D. E., Matthias, M. A., Adhikarla, H., Adler, B., Amorim-Santos, L., Berg, D. E., Bulach, D., Buschiazzo, A., Chang, Y. F., Galloway, R. L., Haake, D. A., Haft, D. H., Hartskeerl, R., Ko, A. I., Levett, P. N., Matsunaga, J., Mechaly, A. E., Monk, J. M., Nascimento, A. L., Nelson, K. E., Palsson, B., Peacock, S. J., Picardeau, M., Ricaldi, J. N., Thaipandungpanit, J., Wunder, E. A. Jr., Yang, X. F., Zhang, J. J. and Vinetz, J. M. (2016). What makes a bacterial species pathogenic?: comparative genomic analysis of the genus Leptospira. PLoS Neglected Tropical Diseases 10, e0004403.CrossRefGoogle ScholarPubMed
Ganoza, C. A., Matthias, M. A., Collins-Richards, D., Brouwer, K. C., Cunningham, C. B., Segura, E. R., Gilman, R. H., Gotuzzo, E. and Vinetz, J. M. (2006). Determining risk for severe leptospirosis by molecular analysis of environmental surface waters for pathogenic Leptospira. PLoS Medicine 3, e308.CrossRefGoogle ScholarPubMed
Gay, N., Soupé-Gilbert, M. E. and Goarant, C. (2014). Though not reservoirs, dogs might transmit Leptospira in New Caledonia. International Journal of Environmental Research and Public Health 11, 4316–4325.Google Scholar
Gerth, M. and Bleidorn, C. (2013). A multilocus sequence typing (MLST) approach to diminish the problems that are associated with DNA barcoding: a reply to Stahlhut etal. (2012). Systematics and Biodiversity 11, 15–17.Google Scholar
Goarant, C. (2016). Leptospirosis: risk factors and management challenges in developing countries. Research and Reports in Tropical Medicine 7, 49–62.Google Scholar
Goarant, C., Colot, J., Faelchlin, E., Ponchet, M., Soupé-Gilbert, M. E., Descloux, E. and Gourinat, A. (2014). An exotic case of leptospirosis imported into an endemic area. Travel Medicine and Infectious Disease 12, 198–200.Google Scholar
Goh, S. H., Potter, S., Wood, J. O., Hemmingsen, S. M., Reynolds, R. P. and Chow, A. W. (1996). HSP60 gene sequences as universal targets for microbial species identification: studies with coagulase-negative staphylococci. Journal of Clinical Microbiology 34, 818–823.CrossRefGoogle ScholarPubMed
Gomard, Y., Dietrich, M., Wieseke, N., Ramasindrazana, B., Lagadec, E., Goodman, S. M., Dellagi, K. and Tortosa, P. (2016). Malagasy bats shelter a considerable genetic diversity of pathogenic Leptospira suggesting notable host-specificity patterns. FEMS Microbiology Ecology 92, fiw037.CrossRefGoogle Scholar
Gravekamp, C., Van de Kemp, H., Franzen, M., Carrington, D., Schoone, G. J., Van Eys, G. J., Everard, C. O., Hartskeerl, R. A. and Terpstra, W. J. (1993). Detection of seven species of pathogenic leptospires by PCR using two sets of primers. Journal of General Microbiology 139, 1691–1700.CrossRefGoogle ScholarPubMed
Guernier, V., Lagadec, E., Cordonin, C., Le Minter, G., Gomard, Y., Pages, F., Jaffar-Bandjee, M. C., Michault, A., Tortosa, P. and Dellagi, K. (2016). Human leptospirosis on Reunion Island, Indian Ocean: are rodents the (only) ones to blame? PLoS Neglected Tropical Diseases 10, e0004733.CrossRefGoogle ScholarPubMed
Haake, D. A. and Levett, P. N. (2015). Leptospirosis in humans. Current Topics in Microbiology and Immunology 387, 65–97.Google Scholar
Haake, D. A., Suchard, M. A., Kelley, M. M., Dundoo, M., Alt, D. P. and Zuerner, R. L. (2004). Molecular evolution and mosaicism of leptospiral outer membrane proteins involves horizontal DNA transfer. Journal of Bacteriology 186, 2818–2828.CrossRefGoogle ScholarPubMed
Halliday, J. E., Knobel, D. L., Allan, K. J., de Bronsvoort, C. B. M., Handel, I., Agwanda, B., Cutler, S. J., Olack, B., Ahmed, A., Hartskeerl, R. A., Njenga, M. K., Cleaveland, S. and Breiman, R. F. (2013). Urban leptospirosis in Africa: a cross-sectional survey of Leptospira infection in rodents in the Kibera Urban Settlement, Nairobi, Kenya. American Journal of Tropical Medicine and Hygiene 89, 1095–1102.CrossRefGoogle Scholar
Hamond, C., Pestana, C. P., Medeiros, M. A. and Lilenbaum, W. (2016). Genotyping of Leptospira directly in urine samples of cattle demonstrates a diversity of species and strains in Brazil. Epidemiology & Infection 144, 72–75.Google Scholar
Harrington, C. S., Moran, L., Ridley, A. M., Newell, D. G. and Madden, R. H. (2003). Inter-laboratory evaluation of three flagellin PCR/RFLP methods for typing Campylobacter jejuni and C. coli: the CAMPYNET experience. Journal of Applied Microbiology 95, 1321–1333.Google Scholar
Hartskeerl, R. A. and Smythe, L. D. (2015). The role of leptospirosis reference laboratories. Current Topics in Microbiology and Immunology 387, 273–288.Google Scholar
Hebert, P. D., Cywinska, A., Ball, S. L. and de Waard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings Biological Sciences 270, 313–321.Google Scholar
Huang, W. M. (1996). Bacterial diversity based on type II DNA topoisomerase genes. Annual Review of Genetics 30, 79–107.CrossRefGoogle ScholarPubMed
Ido, Y., Hoki, R., Ito, H. and Wani, H. (1917). The rat as a carrier of Spirochaeta Icterohaemorrhaguae, the causative agent of Weil's disease (Spirochaetosis Icterohaemorrhagica). Journal of Experimental Medicine 26, 341–353.Google Scholar
Jorge, S., Hartleben, C. P., Seixas, F. K., Coimbra, M. A. A., Stark, C. B., Larrondo, A. G., Amaral, M. G., Albano, A. P. N., Minello, L. F., Dellagostin, O. A. and Brod, C. S. (2012). Leptospira borgpetersenii from free-living white-eared opossum (Didelphis albiventris): first isolation in Brazil. Acta Tropica 124, 147–151.Google Scholar
Kawabata, H., Dancel, L. A., Villanueva, S. Y., Yanagihara, Y., Koizumi, N. and Watanabe, H. (2001). flaB-polymerase chain reaction (flaB-PCR) and its restriction fragment length polymorphism (RFLP) analysis are an efficient tool for detection and identification of Leptospira spp. Microbiology and Immunology 45, 491–496.CrossRefGoogle ScholarPubMed
Kawabata, H., Sakakibara, S., Imai, Y., Masuzawa, T., Fujita, H., Tsurumi, M., Sato, F., Takano, A., Nogami, S., Kaneda, K. and Watanabe, H. (2006). First record of Leptospira borgpetersenii isolation in the Amami Islands, Japan. Microbiology and Immunology 50, 429–434.Google Scholar
Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M. and Glockner, F. O. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research 41, e1.Google Scholar
Koizumi, N., Muto, M., Yamamoto, S., Baba, Y., Kudo, M., Tamae, Y., Shimomura, K., Takatori, I., Iwakiri, A., Ishikawa, K., Soma, H. and Watanabe, H. (2008). Investigation of reservoir animals of Leptospira in the northern part of Miyazaki prefecture. Japanese Journal of Infectious Diseases 61, 465–468.CrossRefGoogle ScholarPubMed
Koizumi, N., Muto, M. M., Akachi, S., Okano, S., Yamamoto, S., Horikawa, K., Harada, S., Funatsumaru, S. and Ohnishi, M. (2013). Molecular and serological investigation of Leptospira and leptospirosis in dogs in Japan. Journal of Medical Microbiology 62, 630–636.Google Scholar
Koren, S., Harhay, G. P., Smith, T. P., Bono, J. L., Harhay, D. M., McVey, S. D., Radune, D., Bergman, N. H. and Phillippy, A. M. (2013). Reducing assembly complexity of microbial genomes with single-molecule sequencing. Genome Biology 14, R101.Google Scholar
Lagadec, E., Gomard, Y., Le Minter, G., Cordonin, C., Cardinale, E., Ramasindrazana, B., Dietrich, M., Goodman, S. M., Tortosa, P. and Dellagi, K. (2016). Identification of Tenrec ecaudatus, a wild mammal introduced to Mayotte Island, as a reservoir of the newly identified human pathogenic Leptospira mayottensis. PLoS Neglected Tropical Diseases 10, e0004933.Google Scholar
La Scola, B., Bui, L. T., Baranton, G., Khamis, A. and Raoult, D. (2006). Partial rpoB gene sequencing for identification of Leptospira species. FEMS Microbiology Letters 263, 142–147.Google Scholar
Lehmann, J. S., Matthias, M. A., Vinetz, J. M. and Fouts, D. E. (2014). Leptospiral pathogenomics. Pathogens 3, 280–308.Google Scholar
Levett, P. N. (2001). Leptospirosis. Clinical Microbiology Reviews 14, 296–326.CrossRefGoogle ScholarPubMed
Levett, P. N. (2015). Systematics of leptospiraceae. Current Topics in Microbiology and Immunology 387, 11–20.Google ScholarPubMed
Levett, P. N., Morey, R. E., Galloway, R. L., Turner, D. E., Steigerwalt, A. G. and Mayer, L. W. (2005). Detection of pathogenic leptospires by real-time quantitative PCR. Journal of Medical Microbiology 54, 45–49.Google Scholar
Levett, P. N., Morey, R. E., Galloway, R. L. and Steigerwalt, A. G. (2006). Leptospira broomii sp. nov., isolated from humans with leptospirosis. International Journal of Systematic and Evolutionary Microbiology 56, 671–673.CrossRefGoogle ScholarPubMed
Lin, T., Oliver, J. H. Jr. and Gao, L. (2004). Molecular characterization of Borrelia isolates from ticks and mammals from the southern United States. Journal of Parasitology 90, 1298–1307.Google Scholar
Links, M. G., Dumonceaux, T. J., Hemmingsen, S. M. and Hill, J. E. (2012). The chaperonin-60 universal target is a barcode for bacteria that enables de novo assembly of metagenomic sequence data. PLoS ONE 7, e49755.Google Scholar
Llanes, A., Restrepo, C. M. and Rajeev, S. (2016). Whole genome sequencing allows better understanding of the evolutionary history of Leptospira interrogans Serovar Hardjo. PLoS ONE 11, e0159387.Google Scholar
Loman, N. J., Quick, J. and Simpson, J. T. (2015). A complete bacterial genome assembled de novo using only nanopore sequencing data. Nature Methods 12, 733–735.Google Scholar
Maiden, M. C., Bygraves, J. A., Feil, E., Morelli, G., Russell, J. E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K., Caugant, D. A., Feavers, I. M., Achtman, M. and Spratt, B. G. (1998). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences of the USA 95, 3140–3145.Google Scholar
Mallo, D. and Posada, D. (2016). Multilocus inference of species trees and DNA barcoding. Philos Trans R Soc Lond B Biol Sci. 371, 1702. pii: 20150335. doi: 10.1098/rstb.2015.0335.Google Scholar
Marshall, R. B. and Manktelow, B. W. (2002). Fifty years of leptospirosis research in New Zealand: a perspective. New Zealand Veterinary Journal 50, 61–63.Google Scholar
Mason, M. R., Encina, C., Sreevatsan, S. and Munoz-Zanzi, C. (2016). Distribution and diversity of pathogenic Leptospira species in peri-domestic surface waters from South Central Chile. PLoS Neglected Tropical Diseases 10, e0004895.Google Scholar
Matthias, M. A., Ricaldi, J. N., Cespedes, M., Diaz, M. M., Galloway, R. L., Saito, M., Steigerwalt, A. G., Patra, K. P., Ore, C. V., Gotuzzo, E., Gilman, R. H., Levett, P. N. and Vinetz, J. M. (2008). Human leptospirosis caused by a new, antigenically unique Leptospira associated with a Rattus species reservoir in the Peruvian Amazon. PLoS Neglected Tropical Diseases 2, e213.Google Scholar
Mayer-Scholl, A., Hammerl, J. A., Schmidt, S., Ulrich, R. G., Pfeffer, M., Woll, D., Scholz, H. C., Thomas, A. and Nockler, K. (2014). Leptospira spp. in rodents and shrews in Germany. International Journal of Environmental Research and Public Health 11, 7562–7574.CrossRefGoogle ScholarPubMed
McBride, A. J., Athanazio, D. A., Reis, M. G. and Ko, A. I. (2005). Leptospirosis. Current Opinion in Infectious Diseases 18, 376–386.Google Scholar
Merien, F., Amouriaux, P., Perolat, P., Baranton, G. and Saint Girons, I. (1992). Polymerase chain reaction for detection of Leptospira spp in clinical samples. Journal of Clinical Microbiology 30, 2219–2224.Google Scholar
Merien, F., Portnoi, D., Bourhy, P., Charavay, F., Berlioz-Arthaud, A. and Baranton, G. (2005). A rapid and quantitative method for the detection of Leptospira species in human leptospirosis. FEMS Microbiology Letters 249, 139–147.Google Scholar
Mgode, G., Mhamphi, G., Katakweba, A., Paemelaere, E., Willekens, N., Leirs, H., Machang'u, R. and Hartskeerl, R. (2005). PCR detection of Leptospira DNA in rodents and insectivores from Tanzania. Belgian Journal of Zoology 135, 17–19.Google Scholar
Mgode, G. F., Machang'u, R. S., Mhamphi, G. G., Katakweba, A., Mulungu, L. S., Durnez, L., Leirs, H., Hartskeerl, R. A. and Belmain, S. R. (2015). Leptospira serovars for diagnosis of leptospirosis in humans and animals in Africa: common Leptospira isolates and reservoir hosts. PLoS Neglected Tropical Diseases 9, e0004251.Google Scholar
Muller, S. K., Assenga, J. A., Matemba, L. E., Misinzo, G. and Kazwala, R. R. (2016). Human leptospirosis in Tanzania: sequencing and phylogenetic analysis confirm that pathogenic Leptospira species circulate among agro-pastoralists living in Katavi-Rukwa ecosystem. BMC Infectious Diseases 16, 273.Google Scholar
Muñoz-Zanzi, C., Mason, M. R., Encina, C., Astroza, A. and Romero, A. (2014). Leptospira contamination in household and environmental water in rural communities in Southern Chile. International Journal of Environmental Research and Public Health 11, 6666–6680.Google Scholar
Nalam, K., Ahmed, A., Devi, S. M., Francalacci, P., Baig, M., Sechi, L. A., Hartskeerl, R. A. and Ahmed, N. (2010). Genetic affinities within a large global collection of pathogenic Leptospira: implications for strain identification and molecular epidemiology. PLoS ONE. 5(8):e12637. doi: 10.1371/journal.pone.0012637.Google Scholar
Obiegala, A., Woll, D., Karnath, C., Silaghi, C., Schex, S., Essbauer, S. and Pfeffer, M. (2016). Prevalence and genotype allocation of pathogenic Leptospira species in small mammals from various habitat types in Germany. PLoS Neglected Tropical Diseases 10, e0004501.CrossRefGoogle ScholarPubMed
Ogawa, H., Koizumi, N., Ohnuma, A., Mutemwa, A., Hang'ombe, B. M., Mweene, A. S., Takada, A., Sugimoto, C., Suzuki, Y., Kida, H. and Sawa, H. (2015). Molecular epidemiology of pathogenic Leptospira spp. in the straw-colored fruit bat (Eidolon helvum) migrating to Zambia from the Democratic Republic of Congo. Infection, Genetics and Evolution 32, 143–147.Google Scholar
Pace, N. R. (1997). A molecular view of microbial diversity and the biosphere. Science 276, 734–740.Google Scholar
Pagès, F., Kuli, B., Moiton, M. P., Goarant, C. and Jaffar-Bandjee, M. C. (2015). Leptospirosis after a stay in Madagascar. Journal of Travel Medicine, 22, 136–139.Google Scholar
Paster, B. J., Dewhirst, F. E., Weisburg, W. G., Tordoff, L. A., Fraser, G. J., Hespell, R. B., Stanton, T. B., Zablen, L., Mandelco, L. and Woese, C. R. (1991). Phylogenetic analysis of the Spirochetes. Journal of Bacteriology 173, 6101–6109.Google Scholar
Perez, J. and Goarant, C. (2010). Rapid Leptospira identification by direct sequencing of the diagnostic PCR products in New Caledonia. BMC Microbiology 10, 325.Google Scholar
Perez, J., Brescia, F., Becam, J., Mauron, C. and Goarant, C. (2011). Rodent abundance dynamics and leptospirosis carriage in an area of hyper-endemicity in New Caledonia. PLoS Neglected Tropical Diseases 5, e1361.Google Scholar
Petersen, A. M., Boye, K., Blom, J., Schlichting, P. and Krogfelt, K. A. (2001). First isolation of Leptospira fainei serovar Hurstbridge from two human patients with Weil's syndrome. Journal of Medical Microbiology 50, 96–100.Google Scholar
Picardeau, M. (2015). Genomics, proteomics, and genetics of Leptospira. Current Topics in Microbiology and Immunology 387, 43–63.Google ScholarPubMed
Picardeau, M., Bulach, D. M., Bouchier, C., Zuerner, R. L., Zidane, N., Wilson, P. J., Creno, S., Kuczek, E. S., Bommezzadri, S., Davis, J. C., McGrath, A., Johnson, M. J., Boursaux-Eude, C., Seemann, T., Rouy, Z., Coppel, R. L., Rood, J. I., Lajus, A., Davies, J. K., Medigue, C. and Adler, B. (2008). Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS ONE 3, e1607.CrossRefGoogle ScholarPubMed
Razzauti, M., Galan, M., Bernard, M., Maman, S., Klopp, C., Charbonnel, N., Vayssier-Taussat, M., Eloit, M. and Cosson, J. F. (2015). A comparison between transcriptome sequencing and 16S metagenomics for detection of bacterial pathogens in wildlife. PLoS Neglected Tropical Diseases 9, e0003929.Google Scholar
Ren, S., Fu, G., Jiang, X.-G., Zeng, R., Miao, Y.-G., Xu, H., Zhang, Y.-X., Xiong, H., Lu, G., Lu, L.-F., Jiang, H.-Q., Jia, J., Tu, Y.-F., Jiang, J.-X., Gu, W.-Y., Zhang, Y.-Q., Cai, Z., Sheng, H.-H., Yin, H.-F., Zhang, Y., Zhu, G.-F., Wan, M., Huang, H.-L., Qian, Z., Wang, S.-Y., Ma, W., Yao, Z.-J., Shen, Y., Qiang, B.-Q., Xia, Q.-C., Guo, X.-K., Danchin, A., Saint Girons, I., Sommerville, R. L., Wen, Y.-M., Shi, M.-H., Chen, Z., Xu, J.-G. and Zhao, G.-P. (2003). Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422, 888–893.Google Scholar
Saint Girons, I., Norris, S. J., Gobel, U., Meyer, J., Walker, E. M. and Zuerner, R. (1992). Genome structure of spirochetes. Research in Microbiology 143, 615–621.Google Scholar
Saito, M., Villanueva, S. Y., Masuzawa, T., Haraguchi, Y., Ita, S., Miyahara, S., Ozuru, R., Yamaguchi, T., Yoshimura, M., Ikejiri, M., Aramaki, N., Amran, M. Y., Muslich, L. T., Iida, K. I., Yanagihara, Y., Gloriani, N. G. and Yoshida, S. I. (2015). The usefulness of semi-solid medium in the isolation of highly virulent Leptospira strains from wild rats in an urban area of Fukuoka, Japan. Microbiology and Immunology 59, 322–330.Google Scholar
Schmid, G. P., Steere, A. C., Kornblatt, A. N., Kaufmann, A. F., Moss, C. W., Johnson, R. C., Hovind-Hougen, K. and Brenner, D. J. (1986). Newly recognized Leptospira species (‘Leptospira inadai’ serovar lyme) isolated from human skin. Journal of Clinical Microbiology, 24, 484–486.Google Scholar
Slack, A. T., Symonds, M. L., Dohnt, M. F. and Smythe, L. D. (2006). Identification of pathogenic Leptospira species by conventional or real-time PCR and sequencing of the DNA gyrase subunit B encoding gene. BMC Microbiology 6, 95.Google Scholar
Slack, A. T., Kalambaheti, T., Symonds, M. L., Dohnt, M. F., Galloway, R. L., Steigerwalt, A. G., Chaicumpa, W., Bunyaraksyotin, G., Craig, S., Harrower, B. J. and Smythe, L. D. (2008). Leptospira wolffii sp. nov., isolated from a human with suspected leptospirosis in Thailand. International Journal of Systematic and Evolutionary Microbiology, 58, 2305–2308.Google Scholar
Smith, M. A., Bertrand, C., Crosby, K., Eveleigh, E. S., Fernandez-Triana, J., Fisher, B. L., Gibbs, J., Hajibabaei, M., Hallwachs, W., Hind, K., Hrcek, J., Huang, D. W., Janda, M., Janzen, D. H., Li, Y., Miller, S. E., Packer, L., Quicke, D., Ratnasingham, S., Rodriguez, J., Rougerie, R., Shaw, M. R., Sheffield, C., Stahlhut, J. K., Steinke, D., Whitfield, J., Wood, M. and Zhou, X. (2012). Wolbachia and DNA barcoding insects: patterns, potential, and problems. PLoS ONE 7, e36514.Google Scholar
Smythe, L. D., Smith, I. L., Smith, G. A., Dohnt, M. F., Symonds, M. L., Barnett, L. J. and McKay, D. B. (2002). A quantitative PCR (TaqMan) assay for pathogenic Leptospira spp. BMC Infectious Diseases 2, 13.Google Scholar
Stoddard, R. A., Gee, J. E., Wilkins, P. P., McCaustland, K. and Hoffmaster, A. R. (2009). Detection of pathogenic Leptospira spp. through TaqMan polymerase chain reaction targeting the LipL32 gene. Diagnostic Microbiology and Infectious Diseases 64, 247–255.Google Scholar
Taylor, H. R. and Harris, W. E. (2012). An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding. Molecular Ecology Resources 12, 377–388.Google Scholar
Thaipadungpanit, J., Wuthiekanun, V., Chierakul, W., Smythe, L. D., Petkanchanapong, W., Limpaiboon, R., Apiwatanaporn, A., Slack, A. T., Suputtamongkol, Y., White, N. J., Feil, E. J., Day, N. P. and Peacock, S. J. (2007). A dominant clone of Leptospira interrogans associated with an outbreak of human leptospirosis in Thailand. PLoS Neglected Tropical Diseases 1, e56.Google Scholar
Thibeaux, R., Geroult, S., Benezech, C., Chabaud, S., Soupé-Gilbert, M. E., Girault, D., Bierque, E. and Goarant, C. (2017). Seeking the environmental source of Leptospirosis reveals durable bacterial viability in river soils. PLoS Neglected Tropical Diseases 11, e0005414.Google Scholar
Tsuboi, M., Koizumi, N., Hayakawa, K., Kanagawa, S., Ohmagari, N. and Kato, Y. (2017). Imported Leptospira licerasiae infection in traveler returning to Japan from Brazil. Emerging Infectious Diseases 23, 548–549.Google Scholar
Urwin, R. and Maiden, M. C. (2003). Multi-locus sequence typing: a tool for global epidemiology. Trends in Microbiology 11, 479–487.Google Scholar
Varni, V., Ruybal, P., Lauthier, J. J., Tomasini, N., Brihuega, B., Koval, A. and Caimi, K. (2014). Reassessment of MLST schemes for Leptospira spp typing worldwide. Infection, Genetics and Evolution 22, 216–222.Google Scholar
Verma, A., Soto, E., Illanes, O., Ghosh, S. and Fuentealba, C. (2015). Detection and genotyping of Leptospira spp. from the kidneys of a seemingly healthy pig slaughtered for human consumption. Journal of Infection in Developing Countries 9, 530–532.Google Scholar
Viau, E. J. and Boehm, A. B. (2011). Quantitative PCR-based detection of pathogenic Leptospira in Hawai'ian coastal streams. Journal of Water and Health 9, 637–646.Google Scholar
Victoria, B., Ahmed, A., Zuerner, R. L., Ahmed, N., Bulach, D. M., Quinteiro, J. and Hartskeerl, R. A. (2008). Conservation of the S10-spc- α locus within otherwise highly plastic genomes provides phylogenetic insight into the genus Leptospira. PLoS ONE 3, e2752.Google Scholar
Villanueva, S. Y. A. M., Saito, M., Baterna, R. A., Estrada, C. A. M., Rivera, A. K. B., Dato, M. C., Zamora, P. R. F. C., Segawa, T., Cavinta, L. L., Fukui, T., Masuzawa, T., Yanagihara, Y., Gloriani, N. G. and Yoshida, S.-I. (2014). Leptospira-rat-human relationship in Luzon, Philippines. Microbes and Infection 16, 902–910.Google Scholar
Weekes, C. C., Everard, C. O. and Levett, P. N. (1997). Seroepidemiology of canine leptospirosis on the island of Barbados. Veterinary Microbiology 57, 215–222.Google Scholar
Weiss, S., Menezes, A., Woods, K., Chanthongthip, A., Dittrich, S., Opoku-Boateng, A., Kimuli, M. and Chalker, V. (2016). An extended multilocus sequence typing (MLST) scheme for rapid direct typing of Leptospira from clinical samples. PLoS Neglected Tropical Diseases 10, e0004996.Google Scholar
Xu, Y., Zhu, Y., Wang, Y., Chang, Y. F., Zhang, Y., Jiang, X., Zhuang, X., Zhu, Y., Zhang, J., Zeng, L., Yang, M., Li, S., Wang, S., Ye, Q., Xin, X., Zhao, G., Zheng, H., Guo, X. and Wang, J. (2016). Whole genome sequencing revealed host adaptation-focused genomic plasticity of pathogenic Leptospira. Scientific Reports 6, 20020.Google Scholar
Zilber, A. L., Picardeau, M., Ayral, F., Artois, M., Demont, P., Kodjo, A. and Djelouadji, Z. (2014). High-resolution typing of Leptospira interrogans by Multispacer Sequence Typing. Journal of Clinical Microbiology 52, 564–571.Google Scholar