[en] [en] BACKGROUND: Yak, a predominant livestock of plateau areas, is known as a host to many parasites. And the genus Entamoeba, the third-common cause of the mortality worldwide from parasitic diseases, was discovered in yaks once.
METHODS: We investigated the distribution and species of Entamoeba spp. from yaks in Qinghai province, northwestern China, by collecting 1027 yak fecal samples. All samples were divided according to seven geographical sites, four seasons, and two age groups of yaks. After extracting DNA, polymerase chain reaction (PCR) was performed to amplify the 18S rRNA gene, and sequences were analyzed with phylogenetic method.
RESULTS: We observed an overall Entamoeba positive rate of 36.32% (373/1027) in yaks from Qinghai province. The common species included Entamoeba bovis (284/373), Entamoeba sp. MG107/BEL (79/373), Entamoeba sp. ribosomal lineage (RL) two (8/373), and Entamoeba sp. RL9 (2/373). According to the result of statistical analysis, Entamoeba infection rate was the highest in summer and significantly differed from that observed during other seasons (P < 0.05). The yaks from Golog had the highest prevalence of Entamoeba among all geographical origins in Qinghai province (P < 0.05). However, no significant difference was observed (P > 0.05) among different age groups, as evident from a positive rate of 39.58% in ≤ 6-month and 36.16% in > 6-month yaks.
CONCLUSION: These results indicate the prevalence and predominant species of Entamoeba in yaks. To our knowledge, this is the first study to report E. bovis, Entamoeba sp. RL2, and Entamoeba sp. RL9 in Chinese yaks.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Ren, Mei ; Université de Liège - ULiège > TERRA Research Centre ; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China ; State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, 810016, Qinghai Province, People's Republic of China ; State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu Province, People's Republic of China
Yang, Fan; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China
Gou, Jing-Min; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China
Wang, Pin-Xue; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China
Zou, Min; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China
Zhong, Xiao-Hong; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China
Lin, Qing ; College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi Province, People's Republic of China. yllinqing@126.com ; State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, 810016, Qinghai Province, People's Republic of China. yllinqing@126.com ; State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, 730046, Gansu Province, People's Republic of China. yllinqing@126.com
Language :
English
Title :
First Detection and Molecular Identification of Entamoeba in Yaks from China.
Publication date :
March 2021
Journal title :
Acta Parasitologica
ISSN :
1230-2821
eISSN :
1896-1851
Publisher :
Springer Science and Business Media Deutschland GmbH, Switzerland
This study was supported by the Key Research and Development Project of Shaanxi Province (Grant number No. 2020NY-017 to QL) and the State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (Grant number No. SKLVEB2019KFKT007 to QL). Acknowledgements
Lan D, Xiong X, Mipam TD, Fu C, Li Q, Ai Y, Hou D, Chai Z, Zhong J, Li J (2018) Genetic diversity, molecular phylogeny and selection evidence of Jinchuan yak revealed by whole-genome resequencing. G3 Bethesda 8(3):945–952. 10.1534/g3.118.300572 DOI: 10.1534/g3.118.300572
Wang G, Wang G, Li X, Zhang X, Karanis G, Jian Y, Ma L, Karanis P (2018) Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in 1–2-month-old highland yaks in Qinghai Province China. Parasitol Res 117(6):1793–1800. 10.1007/s00436-018-5861-3 DOI: 10.1007/s00436-018-5861-3
Qin SY, Zhou DH, Cong W, Zhang XX, Lou ZL, Yin MY, Tan QD, Zhu XQ (2015) Seroprevalence, risk factors and genetic characterization of Toxoplasma gondii in free-range white yaks (Bos grunniens) in China. Vet Parasitol 211(3–4):300–302. 10.1016/j.vetpar.2015.05.015 DOI: 10.1016/j.vetpar.2015.05.015
Feng M, Cai J, Min X, Fu Y, Xu Q, Tachibana H, Cheng X (2013) Prevalence and genetic diversity of Entamoeba species infecting macaques in southwest China. Parasitol Res 112(4):1529–1536. 10.1007/s00436-013-3299-1 DOI: 10.1007/s00436-013-3299-1
Ma J, Cai J, Ma J, Feng Y, Xiao L (2015) Enterocytozoon bieneusi genotypes in yaks (Bos grunniens) and their public health potential. J Eukaryot Microbiol 62(1):21–25. 10.1111/jeu.12141 DOI: 10.1111/jeu.12141
Wang GH, Wang GP, Li XP, Ma LQ, Karanis G, Christodoulou-Vafeiadou E, Karanis P (2017) Detection of Giardia duodenalis assemblage E infections at the Tibetan Plateau Area: yaks are suitable hosts. Acta Trop 169:157–162. 10.1016/j.actatropica.2017.02.018 DOI: 10.1016/j.actatropica.2017.02.018
Li K, Jiang J, Shahzad M, Zhang H, Mehmood K, Jiang X, Zhao XD, Luo HQ, Tong XL, Li JK (2018) Revealing the parasitic infection in diarrheic yaks by piloting high-throughput sequencing. Microb Pathog 117:153–156. 10.1016/j.micpath.2018.02.033 DOI: 10.1016/j.micpath.2018.02.033
Shilton CM, Šlapeta J, Shine R, Brown GP (2019) Pathology associated with an outbreak of Entamoebiasis in Wild Cane Toads (Rhinella marina) in tropical Australia. Vet Pathol 56(6):921–931. 10.1177/0300985819868729 DOI: 10.1177/0300985819868729
Jinatham V, Popluechai S, Clark CG, Gentekaki E (2019) Entamoeba chiangraiensis N. Sp. (Amoebozoa: Entamoebidae) isolated from the gut of Asian Swamp Eel (Monopterus albus) in Northern Thailand. Parasitology 146(14):1719–1724. 10.1017/S0031182019000775 DOI: 10.1017/S0031182019000775
Kawano T, Imada M, Chamavit P, Kobayashi S, Hashimoto T, Nozaki T (2017) Genetic diversity of Entamoeba: novel ribosomal lineages from cockroaches. PLoS ONE 12(9):e0185233. 10.1371/journal.pone.0185233 DOI: 10.1371/journal.pone.0185233
Noble GA, Noble ER (1952) Entamoebae in farm mammals. J Parasitol 38(6):571–595 DOI: 10.2307/3273985
Kingston N, Stabler RM (1978) Two species of Entamoeba from white-tailed deer, Odocoileus virginianus, from Georgia. J Parasitol 64(1):14–16 DOI: 10.2307/3279600
Silberman JD, Clark CG, Diamond LS, Sogin ML (1999) Phylogeny of the genera Entamoeba and Endolimax as deduced from small-subunit ribosomal RNA sequences. Mol Biol Evol 16(12):1740–1751. 10.1093/oxfordjournals.molbev.a026086 DOI: 10.1093/oxfordjournals.molbev.a026086
Verweij JJ, Polderman AM, Clark CG (2001) Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. J Clin Microbiol 39(4):1644–1646. 10.1128/JCM.39.4.1644-1646.2001 DOI: 10.1128/JCM.39.4.1644-1646.2001
Clark CG, Kaffashian F, Tawari B, Windsor JJ, Twiggflesner A, Daviesmorel MC, Blessmann J, Ebert F, Peschel B, Le Van A, Jackson CJ (2006) New insights into the phylogeny of Entamoeba species provided by analysis of four new small-subunit rRNA genes. Int J Syst Evol Microbiol 56(Pt 9):2235–2239. 10.1099/ijs.0.64208-0 DOI: 10.1099/ijs.0.64208-0
Skirnisson K, Hansson H (2006) Causes of diarrhoea in lambs during autumn and early winter in an icelandic flock of sheep. Icel Agric Sci 19:43–57
Jacob AS, Busby EJ, Levy AD, Komm N, Clark CG (2016) Expanding the Entamoeba universe: new hosts yield novel ribosomal lineages. J Eukaryot Microbiol 63(1):69–78. 10.1111/jeu.12249 DOI: 10.1111/jeu.12249
Wilson IW, Weedall GD, Lorenzi H, Howcroft T, Hon CC, Deloger M, Guillén N, Paterson S, Clark CG, Hall N (2019) Genetic diversity and gene family expansions in members of the genus Entamoeba. Genome Biol Evol 11(3):688–705. 10.1093/gbe/evz009 DOI: 10.1093/gbe/evz009
Stensvold CR, Lebbad M, Clark CG (2010) Genetic characterisation of uninucleated cyst-producing Entamoeba spp. from ruminants. Int J Parasitol 40(7):775–778. 10.1016/j.ijpara.2010.03.003 DOI: 10.1016/j.ijpara.2010.03.003
Stensvold CR, Lebbad M, Victory EL, Verweij JJ, Tannich E, Alfellani M, Legarraga P, Clark CG (2011) Increased sampling reveals novel lineages of Entamoeba: consequences of genetic diversity and host specificity for taxonomy and molecular detection. Protist 162(3):525–541. 10.1016/j.protis.2010.11.002 DOI: 10.1016/j.protis.2010.11.002
Mackinnon DL, Dibb MJ (1938) Report on intestinal protozoa of some mammals in the Zoological Gardens at Regent’s Park. Proc of the Zool Soc London B 108:323–346
Bray RS (1964) A check-list of the parasitic protozoa of west Africa with some notes on their classification. Bull Inst Fr Afr Noire 26(1):238–315
Al-Habsi K, Yang R, Ryan U, Jacobson C, Miller DW (2017) Morphological and molecular characterization of an uninucleated cyst-producing Entamoeba, spp. in captured Rangeland goats in Western Australia. Vet Parasitol 235:41–46. 10.1016/j.vetpar.2017.01.013 DOI: 10.1016/j.vetpar.2017.01.013
Jiménez AE, Montenegro VM, Hernández J, Dolz G, Maranda L, Galindo J, Epe C, Schnieder T (2007) Dynamics of infections with gastrointestinal parasites and Dictyocaulus viviparus in dairy and beef cattle from Costa Rica. Vet Parasitol 148(3–4):262–271. 10.1016/j.vetpar.2007.06.015 DOI: 10.1016/j.vetpar.2007.06.015
Nolan MJ, Unger M, Yeap YT, Rogers E, Millet I, Harman K, Fox M, Kalema-Zikusoka G, Blake DP (2017) Molecular characterisation of protist parasites in human-habituated mountain gorillas (Gorilla beringei beringei), humans and livestock, from Bwindi impenetrable National park Uganda. Parasit Vectors 10(1):340. 10.1186/s13071-017-2283-5 DOI: 10.1186/s13071-017-2283-5
Matsubayashi M, Matsuura Y, Nukata S, Daizi Y, Shibahara T, Teramoto I, Matsuo T, Uni S, Hatta T, Kaneko A et al (2017) First detection and molecular identification of Entamoeba bovis from Japanese cattle. Parasitol Res 117(1):339–342. 10.1007/s00436-017-5689-2 DOI: 10.1007/s00436-017-5689-2
Verweij JJ, Laeijendecker D, Brienen EA, Van LL, Polderman AM (2003) Detection and identification of Entamoeba species in stool samples by a reverse line hybridization assay. J Clin Microbiol 41(11):5041–5045. 10.1128/jcm.41.11.5041-5045.2003 DOI: 10.1128/jcm.41.11.5041-5045.2003
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. 10.1093/nar/25.24.4876 DOI: 10.1093/nar/25.24.4876
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. 10.1093/molbev/msw054 DOI: 10.1093/molbev/msw054
Guan Y, Feng M, Cai J, Min X, Zhou X, Xu Q, Tan N, Cheng X, Tachibana H (2016) Comparative analysis of genotypic diversity in Entamoeba nuttalli isolates from Tibetan macaques and rhesus macaques in China. Infect Genet Evol 38:126–131. 10.1016/j.meegid.2015.12.014 DOI: 10.1016/j.meegid.2015.12.014
Yang B, Chen Y, Wu L, Xu L, Tachibana H, Cheng X (2012) Seroprevalence of Entamoeba histolytica infection in China. Am J Trop Med Hyg 87(1):97–103. 10.4269/ajtmh.2012.11-0626 DOI: 10.4269/ajtmh.2012.11-0626
Zhang XP, He YY, Wang ZY, Zhang YG, Zhu Q, Jiang SF, Li Y, Cheng YP, Yin MM (2015) Investigation on Entamoeba histolytica infection in diarrhea patients from general hospitals in Shanghai City. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 27(6):600–603. 10.16250/j.32.1374.2015210 DOI: 10.16250/j.32.1374.2015210
Villamizar X, Higuera A, Herrera G, Vasquez-A LR, Buitron L, Muñoz LM, Gonzalez-C FE, Lopez MC, Giraldo JC, Ramírez JD (2019) Molecular and descriptive epidemiology of intestinal protozoan parasites of children and their pets in Cauca, Colombia: a cross-sectional study. BMC Infect Dis 19(1):190. 10.1186/s12879-019-3810-0 DOI: 10.1186/s12879-019-3810-0
Yang ZQ, Zuo YX, Yao YG, Chen XW, Yang GC, Zhang YP (2001) Analysis of the 18s rRNA genes of Sarcocystis species suggests that the morphologically similar organisms from cattle and water buffalo should be considered the same species. Mol Biochem Parasitol 115(2):283–288. 10.1016/s0166-6851(01)00283-3 DOI: 10.1016/s0166-6851(01)00283-3
Moreno Y, Moreno-Mesonero L, Amorós I, Pérez R, Morillo JA, Alonso JL (2018) Multiple identification of most important waterborne protozoa in surface water used for irrigation purposes by 18s rRNA amplicon-based metagenomics. Int J Hyg Environ Health 221(1):102–111. 10.1016/j.ijheh.2017.10.008 DOI: 10.1016/j.ijheh.2017.10.008