Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau

IntroductionTicks and fleas, as blood-sucking arthropods, carry and transmit various zoonotic diseases. In the natural plague foci of China, monitoring of Yersinia pestis has been continuously conducted in Marmota himalayana and other host animals, whereas other pathogens carried by vectors are rare...

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Main Authors: Lingzhi Dong, Yaben Li, Caixin Yang, Jian Gong, Wentao Zhu, Yuyuan Huang, Mimi Kong, Lijun Zhao, Feifei Wang, Shan Lu, Ji Pu, Jing Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1188155/full
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author Lingzhi Dong
Lingzhi Dong
Yaben Li
Yaben Li
Caixin Yang
Caixin Yang
Jian Gong
Jian Gong
Wentao Zhu
Yuyuan Huang
Mimi Kong
Mimi Kong
Lijun Zhao
Lijun Zhao
Feifei Wang
Feifei Wang
Shan Lu
Shan Lu
Shan Lu
Ji Pu
Ji Pu
Jing Yang
Jing Yang
Jing Yang
author_facet Lingzhi Dong
Lingzhi Dong
Yaben Li
Yaben Li
Caixin Yang
Caixin Yang
Jian Gong
Jian Gong
Wentao Zhu
Yuyuan Huang
Mimi Kong
Mimi Kong
Lijun Zhao
Lijun Zhao
Feifei Wang
Feifei Wang
Shan Lu
Shan Lu
Shan Lu
Ji Pu
Ji Pu
Jing Yang
Jing Yang
Jing Yang
author_sort Lingzhi Dong
collection DOAJ
description IntroductionTicks and fleas, as blood-sucking arthropods, carry and transmit various zoonotic diseases. In the natural plague foci of China, monitoring of Yersinia pestis has been continuously conducted in Marmota himalayana and other host animals, whereas other pathogens carried by vectors are rarely concerned in the Qinghai-Tibet Plateau.MethodsIn this study, we investigated the microbiota of ticks and fleas sampling from M. himalayana in the Qinghai-Tibet Plateau, China by metataxonomics combined with metagenomic methods.ResultsBy metataxonomic approach based on full-length 16S rDNA amplicon sequencing and operational phylogenetic unit (OPU) analyses, we described the microbiota community of ticks and fleas at the species level, annotated 1,250 OPUs in ticks, including 556 known species and 492 potentially new species, accounting for 48.50% and 41.71% of the total reads in ticks, respectively. A total of 689 OPUs were detected in fleas, consisting of 277 known species (40.62% of the total reads in fleas) and 294 potentially new species (56.88%). At the dominant species categories, we detected the Anaplasma phagocytophilum (OPU 421) and potentially pathogenic new species of Wolbachia, Ehrlichia, Rickettsia, and Bartonella. Using shotgun sequencing, we obtained 10 metagenomic assembled genomes (MAGs) from vector samples, including a known species (Providencia heimbachae DFT2), and six new species affliated to four known genera, i.e., Wolbachia, Mumia, Bartonella, and Anaplasma. By the phylogenetic analyses based on full-length 16S rRNA genes and core genes, we identified that ticks harbored pathogenic A. phagocytophilum. Moreover, these potentially pathogenic novel species were more closely related to Ehrlichia muris, Ehrlichia muris subsp. eauclairensis, Bartonella rochalimae, and Rickettsia limoniae, respectively. The OPU 422 Ehrlichia sp1 was most related to Ehrlichia muris and Ehrlichia muris subsp. eauclairensis. The OPU 230 Bartonella sp1 and Bartonella spp. (DTF8 and DTF9) was clustered with Bartonella rochalimae. The OPU 427 Rickettsia sp1 was clustered with Rickettsia limoniae.DiscussionThe findings of the study have advanced our understanding of the potential pathogen groups of vectors in marmot (Marmota himalayana) in the Qinghai-Tibet Plateau.
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spelling doaj.art-576dd066ec814049ab9809e01d4c0a402023-06-21T08:39:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-06-011410.3389/fmicb.2023.11881551188155Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet PlateauLingzhi Dong0Lingzhi Dong1Yaben Li2Yaben Li3Caixin Yang4Caixin Yang5Jian Gong6Jian Gong7Wentao Zhu8Yuyuan Huang9Mimi Kong10Mimi Kong11Lijun Zhao12Lijun Zhao13Feifei Wang14Feifei Wang15Shan Lu16Shan Lu17Shan Lu18Ji Pu19Ji Pu20Jing Yang21Jing Yang22Jing Yang23Department of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Infectious Diseases and Clinical Microbiology, Beijing Chao-Yang Hospital, Capital Medical University, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaResearch Units of Discovery of Unknown Bacteria and Function, Chinese Academy of Medical Sciences, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaDepartment of Epidemiology, School of Public Health, Shanxi Medical University, Taiyuan, ChinaState Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, National Institute for Communicable Disease Control and Prevention, Beijing, ChinaResearch Units of Discovery of Unknown Bacteria and Function, Chinese Academy of Medical Sciences, Beijing, ChinaIntroductionTicks and fleas, as blood-sucking arthropods, carry and transmit various zoonotic diseases. In the natural plague foci of China, monitoring of Yersinia pestis has been continuously conducted in Marmota himalayana and other host animals, whereas other pathogens carried by vectors are rarely concerned in the Qinghai-Tibet Plateau.MethodsIn this study, we investigated the microbiota of ticks and fleas sampling from M. himalayana in the Qinghai-Tibet Plateau, China by metataxonomics combined with metagenomic methods.ResultsBy metataxonomic approach based on full-length 16S rDNA amplicon sequencing and operational phylogenetic unit (OPU) analyses, we described the microbiota community of ticks and fleas at the species level, annotated 1,250 OPUs in ticks, including 556 known species and 492 potentially new species, accounting for 48.50% and 41.71% of the total reads in ticks, respectively. A total of 689 OPUs were detected in fleas, consisting of 277 known species (40.62% of the total reads in fleas) and 294 potentially new species (56.88%). At the dominant species categories, we detected the Anaplasma phagocytophilum (OPU 421) and potentially pathogenic new species of Wolbachia, Ehrlichia, Rickettsia, and Bartonella. Using shotgun sequencing, we obtained 10 metagenomic assembled genomes (MAGs) from vector samples, including a known species (Providencia heimbachae DFT2), and six new species affliated to four known genera, i.e., Wolbachia, Mumia, Bartonella, and Anaplasma. By the phylogenetic analyses based on full-length 16S rRNA genes and core genes, we identified that ticks harbored pathogenic A. phagocytophilum. Moreover, these potentially pathogenic novel species were more closely related to Ehrlichia muris, Ehrlichia muris subsp. eauclairensis, Bartonella rochalimae, and Rickettsia limoniae, respectively. The OPU 422 Ehrlichia sp1 was most related to Ehrlichia muris and Ehrlichia muris subsp. eauclairensis. The OPU 230 Bartonella sp1 and Bartonella spp. (DTF8 and DTF9) was clustered with Bartonella rochalimae. The OPU 427 Rickettsia sp1 was clustered with Rickettsia limoniae.DiscussionThe findings of the study have advanced our understanding of the potential pathogen groups of vectors in marmot (Marmota himalayana) in the Qinghai-Tibet Plateau.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1188155/fulltickfleaMarmota himalayanaAnaplasma phagocytophilumWolbachiaBartonella
spellingShingle Lingzhi Dong
Lingzhi Dong
Yaben Li
Yaben Li
Caixin Yang
Caixin Yang
Jian Gong
Jian Gong
Wentao Zhu
Yuyuan Huang
Mimi Kong
Mimi Kong
Lijun Zhao
Lijun Zhao
Feifei Wang
Feifei Wang
Shan Lu
Shan Lu
Shan Lu
Ji Pu
Ji Pu
Jing Yang
Jing Yang
Jing Yang
Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau
Frontiers in Microbiology
tick
flea
Marmota himalayana
Anaplasma phagocytophilum
Wolbachia
Bartonella
title Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau
title_full Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau
title_fullStr Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau
title_full_unstemmed Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau
title_short Species-level microbiota of ticks and fleas from Marmota himalayana in the Qinghai-Tibet Plateau
title_sort species level microbiota of ticks and fleas from marmota himalayana in the qinghai tibet plateau
topic tick
flea
Marmota himalayana
Anaplasma phagocytophilum
Wolbachia
Bartonella
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1188155/full
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