Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.

Background Leptospirosis, a zoonosis caused by species in the spirochete genus Leptospira, is endemic to the Yaeyama region in Okinawa, subtropical Japan. Species of the P1 subclade "virulent" group, within the genus Leptospira, are the main etiological agents of leptospirosis in Okinawa....

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Published in:PLOS Neglected Tropical Diseases
Main Authors: Yukuto Sato, Idam Hermawan, Tetsuya Kakita, Sho Okano, Hideyuki Imai, Hiroto Nagai, Ryosuke Kimura, Tetsu Yamashiro, Tadashi Kajita, Claudia Toma
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2022
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Online Access:https://doi.org/10.1371/journal.pntd.0010234
https://doaj.org/article/33048f5a476e4d809738c0999d4308a5
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spelling ftdoajarticles:oai:doaj.org/article:33048f5a476e4d809738c0999d4308a5 2023-05-15T15:15:36+02:00 Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan. Yukuto Sato Idam Hermawan Tetsuya Kakita Sho Okano Hideyuki Imai Hiroto Nagai Ryosuke Kimura Tetsu Yamashiro Tadashi Kajita Claudia Toma 2022-03-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0010234 https://doaj.org/article/33048f5a476e4d809738c0999d4308a5 EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0010234 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0010234 https://doaj.org/article/33048f5a476e4d809738c0999d4308a5 PLoS Neglected Tropical Diseases, Vol 16, Iss 3, p e0010234 (2022) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2022 ftdoajarticles https://doi.org/10.1371/journal.pntd.0010234 2022-12-30T21:41:39Z Background Leptospirosis, a zoonosis caused by species in the spirochete genus Leptospira, is endemic to the Yaeyama region in Okinawa, subtropical Japan. Species of the P1 subclade "virulent" group, within the genus Leptospira, are the main etiological agents of leptospirosis in Okinawa. However, their environmental persistence is poorly understood. This study used a combination of bacterial isolation and environmental DNA (eDNA) metabarcoding methods to understand the eco-epidemiology of leptospirosis in this endemic region. Findings Polymerase chain reaction (PCR) characterized twelve human clinical L. interrogans isolates belonging to the P1 subclade "virulent" subgroup and 11 environmental soil isolates of the P1subclade "low virulent" subgroup (genetically related to L. kmetyi, n = 1; L. alstonii, n = 4; L. barantonii, n = 6) from the Yaeyama region targeting four virulence-related genes (lipL32, ligA, ligB and lpxD1). Clinical isolates were PCR positive for at least three targeted genes, while all environmental isolates were positive only for lipL32. Analysis of infected renal epithelial cells with selected clinical and environmental strains, revealed the disassembly of cell-cell junctions for the Hebdomadis clinical strain serogroup. Comparison of leptospiral eDNA during winter and summer identified operational taxonomic units corresponding to the species isolated from soil samples (L. kmetyi and L. barantonii) and additional P2 subclade species (L. licerasiae, L. wolffii-related, among others) that were not detected by soil cultivation. Total Leptospira read counts were higher in summer than in winter and the analysis of leptospiral/animal eDNA relationship suggested Rattus spp. as a potential reservoir animal. Conclusion Our study demonstrated high environmental Leptospira diversity in the Yaeyama region, particularly during summer, when most of the leptospirosis cases are reported. In addition, several Leptospira species with pathogenic potential were identified that have not yet been reported in ... Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 16 3 e0010234
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Yukuto Sato
Idam Hermawan
Tetsuya Kakita
Sho Okano
Hideyuki Imai
Hiroto Nagai
Ryosuke Kimura
Tetsu Yamashiro
Tadashi Kajita
Claudia Toma
Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description Background Leptospirosis, a zoonosis caused by species in the spirochete genus Leptospira, is endemic to the Yaeyama region in Okinawa, subtropical Japan. Species of the P1 subclade "virulent" group, within the genus Leptospira, are the main etiological agents of leptospirosis in Okinawa. However, their environmental persistence is poorly understood. This study used a combination of bacterial isolation and environmental DNA (eDNA) metabarcoding methods to understand the eco-epidemiology of leptospirosis in this endemic region. Findings Polymerase chain reaction (PCR) characterized twelve human clinical L. interrogans isolates belonging to the P1 subclade "virulent" subgroup and 11 environmental soil isolates of the P1subclade "low virulent" subgroup (genetically related to L. kmetyi, n = 1; L. alstonii, n = 4; L. barantonii, n = 6) from the Yaeyama region targeting four virulence-related genes (lipL32, ligA, ligB and lpxD1). Clinical isolates were PCR positive for at least three targeted genes, while all environmental isolates were positive only for lipL32. Analysis of infected renal epithelial cells with selected clinical and environmental strains, revealed the disassembly of cell-cell junctions for the Hebdomadis clinical strain serogroup. Comparison of leptospiral eDNA during winter and summer identified operational taxonomic units corresponding to the species isolated from soil samples (L. kmetyi and L. barantonii) and additional P2 subclade species (L. licerasiae, L. wolffii-related, among others) that were not detected by soil cultivation. Total Leptospira read counts were higher in summer than in winter and the analysis of leptospiral/animal eDNA relationship suggested Rattus spp. as a potential reservoir animal. Conclusion Our study demonstrated high environmental Leptospira diversity in the Yaeyama region, particularly during summer, when most of the leptospirosis cases are reported. In addition, several Leptospira species with pathogenic potential were identified that have not yet been reported in ...
format Article in Journal/Newspaper
author Yukuto Sato
Idam Hermawan
Tetsuya Kakita
Sho Okano
Hideyuki Imai
Hiroto Nagai
Ryosuke Kimura
Tetsu Yamashiro
Tadashi Kajita
Claudia Toma
author_facet Yukuto Sato
Idam Hermawan
Tetsuya Kakita
Sho Okano
Hideyuki Imai
Hiroto Nagai
Ryosuke Kimura
Tetsu Yamashiro
Tadashi Kajita
Claudia Toma
author_sort Yukuto Sato
title Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.
title_short Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.
title_full Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.
title_fullStr Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.
title_full_unstemmed Analysis of human clinical and environmental Leptospira to elucidate the eco-epidemiology of leptospirosis in Yaeyama, subtropical Japan.
title_sort analysis of human clinical and environmental leptospira to elucidate the eco-epidemiology of leptospirosis in yaeyama, subtropical japan.
publisher Public Library of Science (PLoS)
publishDate 2022
url https://doi.org/10.1371/journal.pntd.0010234
https://doaj.org/article/33048f5a476e4d809738c0999d4308a5
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 16, Iss 3, p e0010234 (2022)
op_relation https://doi.org/10.1371/journal.pntd.0010234
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0010234
https://doaj.org/article/33048f5a476e4d809738c0999d4308a5
op_doi https://doi.org/10.1371/journal.pntd.0010234
container_title PLOS Neglected Tropical Diseases
container_volume 16
container_issue 3
container_start_page e0010234
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