{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T17:09:02Z","timestamp":1785431342930,"version":"3.56.0"},"reference-count":35,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2026,6,9]],"date-time":"2026-06-09T00:00:00Z","timestamp":1780963200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82260659"],"award-info":[{"award-number":["82260659"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["82260659"],"award-info":[{"award-number":["82260659"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>To determine whether Yersinia pestis (Y. pestis) signals were present in the soil, 78 soil samples were collected from 10 counties identified as Rattus tanezumi plague foci and another six counties in non-foci areas in Yunnan, China, from August 2024 to May 2025. Nucleic acids were extracted using the DNeasy PowerSoil Pro Kit (Qiagen) and detected with a Bio-Rad QX200 droplet digital PCR (ddPCR) system targeting two Y. pestis genes (caf1 and ypo0392). Our sampling design also considered two additional dimensions: nine soil types and three habitat types. The raw data obtained from ddPCR were copy numbers. A gene was considered positive when its copy number exceeded the limit of detection (LoD). A sample was considered positive if the copy number of ypo0392 exceeded its LoD (regardless of caf1), or if both genes exceeded their respective LoDs. No correlation was detected between the positivity rate of Y. pestis and the division of sampling sites into plague focus and non-focus regions (p = 0.758). Similarly, the Mann\u2013Whitney U test revealed non-significant differences in pathogen copy number across the two site categories, with p = 0.603 for the caf1 gene and p = 0.372 for the ypo0392 gene. No statistical difference in positivity rate was found for either soil types or habitat types. However, for both the grouping variables, a statistical difference in copy number was observed. Our results indicated that quantifying nucleic acid abundance by copy number provided richer information than a simple positive\/negative determination. The detection of Y. pestis signals was associated with soil type, rather than with whether an area was classified as a focus or non-focus region. Accordingly, future research on the preservation mechanism of Y. pestis should not be restricted to the concept of natural foci but should adopt a broader perspective.<\/jats:p>","DOI":"10.3390\/pathogens15060616","type":"journal-article","created":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T09:25:17Z","timestamp":1781083517000},"page":"616","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Abundance of Yersinia pestis Nucleic Acids in Soil from Rattus tanezumi Plague Foci in Yunnan Using ddPCR"],"prefix":"10.3390","volume":"15","author":[{"given":"Yongmei","family":"La","sequence":"first","affiliation":[{"name":"School of Public Health, Dali University, Dali 671000, China"},{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fan","family":"Li","sequence":"additional","affiliation":[{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"},{"name":"School of Public Health, Kunming Medical University, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cunjuan","family":"Duan","sequence":"additional","affiliation":[{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jinjiao","family":"Kong","sequence":"additional","affiliation":[{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haipeng","family":"Zhang","sequence":"additional","affiliation":[{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongli","family":"Tan","sequence":"additional","affiliation":[{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baoxiang","family":"Li","sequence":"additional","affiliation":[{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youhong","family":"Zhong","sequence":"additional","affiliation":[{"name":"School of Public Health, Dali University, Dali 671000, China"},{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shilong","family":"Yang","sequence":"additional","affiliation":[{"name":"Longchuan County Centre of Diseases Control and Prevention, Dehong Dai and Jingpo Autonomous Prefecture 678700, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3350-1835","authenticated-orcid":false,"given":"Peng","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Public Health, Dali University, Dali 671000, China"},{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5065-7543","authenticated-orcid":false,"given":"Liyuan","family":"Shi","sequence":"additional","affiliation":[{"name":"School of Public Health, Dali University, Dali 671000, China"},{"name":"Yunnan Provincial Key Laboratory of Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Kunming 650500, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,6,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"10214","DOI":"10.1073\/pnas.1019486108","article-title":"Nonlinear Effect of Climate on Plague during the Third Pandemic in China","volume":"108","author":"Xu","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1073\/pnas.1205750110","article-title":"Historical Variations in Mutation Rate in an Epidemic Pathogen, Yersinia pestis","volume":"110","author":"Cui","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1038\/s42003-023-05186-2","article-title":"Genomic Diversity of Yersinia pestis from Yunnan Province, China, Implies a Potential Common Ancestor as the Source of Two Plague Epidemics","volume":"6","author":"Qin","year":"2023","journal-title":"Commun. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e0166222","DOI":"10.1128\/spectrum.01662-22","article-title":"Epidemiological Characteristics of Human and Animal Plague in Yunnan Province, China, 1950 to 2020","volume":"10","author":"Han","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Shi, L., Yang, G., Zhang, Z., Xia, L., Liang, Y., Tan, H., He, J., Xu, J., Song, Z., and Li, W. (2018). Reemergence of Human Plague in Yunnan, China in 2016. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0198067"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Su, C., Duan, B., Duan, Q., He, Z., Sha, H., Liang, Y., Pu, E., Qin, S., Duan, R., and Lyu, D. (2024). Status and Analysis of Undetected Plague Cases in Yunnan Province, China. Front. Public Health, 12.","DOI":"10.3389\/fpubh.2024.1408025"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Li, R., Su, C., Lou, Z., Song, Z., Pu, E., Li, Y., and Gao, Z. (2023). Associations between Ecological Diversity and Rodent Plague Circulation in Yunnan Province, China, 1983\u20132020: A Data-Informed Modelling Study. PLoS Negl. Trop. Dis., 17.","DOI":"10.1371\/journal.pntd.0011317"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Ai, Z.-Q., Li, R., Zhang, Y., Wu, L., Luo, Y.-Y., Hong, R.-D., and Yin, J.-X. (2026). Soil Characteristics Associated with Historical Commensal Rodent Plague Foci in Yunnan Province, China. Front. Vet. Sci., 13.","DOI":"10.3389\/fvets.2026.1797277"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2865","DOI":"10.1099\/mic.0.2007\/016154-0","article-title":"Long-Term Persistence of Virulent Yersinia pestis in Soil","volume":"154","author":"Ayyadurai","year":"2008","journal-title":"Microbiology"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Long, Y., Zhong, Y., Liu, P., Mao, C., Zhang, H., Shi, L., Zi, S., Qin, X., Shao, Z., and Cao, R. (2025). A Novel, Broad-Spectrum, Virulent Bacteriophage Targeting Yersinia pestis Isolated from the Soil of Wild Rodent Nests in Yunnan Province, China. Pathogens, 14.","DOI":"10.3390\/pathogens14121195"},{"key":"ref_11","first-page":"780","article-title":"Establishment of a method for isolating plague phage from soil samples","volume":"34","author":"Li","year":"2018","journal-title":"Chin. J. Pest Control"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"10597","DOI":"10.1007\/s00253-016-7950-5","article-title":"Efficiency and Sensitivity of the Digital Droplet PCR for the Quantification of Antibiotic Resistance Genes in Soils and Organic Residues","volume":"100","author":"Brothier","year":"2016","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Zhao, Y., Yan, Z., Song, K., Li, Y., Shen, L., Cui, Y., Du, Z., Yang, R., Song, Y., and Jing, L. (2024). Development and Evaluation of a Multi-Target Droplet Digital PCR Assay for Highly Sensitive and Specific Detection of Yersinia pestis. PLoS Negl. Trop. Dis., 18.","DOI":"10.1371\/journal.pntd.0012167"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Du, Y., Yan, Z., Song, K., Jin, J., Xiao, L., Sun, Z., Tan, Y., Zhang, P., Du, Z., and Yang, R. (2022). Development and Evaluation of a Multiplex Droplet Digital Polymerase Chain Reaction Method for Simultaneous Detection of Five Biothreat Pathogens. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.970973"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"107926","DOI":"10.1016\/j.marenvres.2026.107926","article-title":"Testing the Waters: A Comparison of DNA Extraction Methods for the Metabarcoding of Microbial Communities","volume":"217","author":"Reaume","year":"2026","journal-title":"Mar. Environ. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1094\/PDIS-03-19-0584-RE","article-title":"Quantification of Plasmodiophora brassicae Resting Spores in Soils Using Droplet Digital PCR (ddPCR)","volume":"104","author":"Wen","year":"2020","journal-title":"Plant Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1038\/s41586-022-04800-3","article-title":"The Source of the Black Death in Fourteenth-Century Central Eurasia","volume":"606","author":"Spyrou","year":"2022","journal-title":"Nature"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"106787","DOI":"10.1016\/j.isci.2023.106787","article-title":"Improving the Extraction of Ancient Yersinia pestis Genomes from the Dental Pulp","volume":"26","author":"Clavel","year":"2023","journal-title":"iScience"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/j.cell.2015.10.009","article-title":"Early Divergent Strains of Yersinia pestis in Eurasia 5000 Years Ago","volume":"163","author":"Rasmussen","year":"2015","journal-title":"Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"102025","DOI":"10.1016\/j.cimid.2023.102025","article-title":"Natural Foci of Plague in Kazakhstan in the Space-Time Continuum","volume":"100","author":"Abdel","year":"2023","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1016\/j.cmi.2016.08.031","article-title":"Molecular History of Plague","volume":"22","author":"Drancourt","year":"2016","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"941","DOI":"10.3201\/eid1406.080029","article-title":"Persistence of Yersinia pestis in Soil Under Natural Conditions","volume":"14","author":"Eisen","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1111\/j.1556-4029.2006.00131.x","article-title":"Environmental Survey for Four Pathogenic Bacteria and Closely Related Species Using Phylogenetic and Functional Genes","volume":"51","author":"Kuske","year":"2006","journal-title":"J. Forensic. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4182","DOI":"10.1002\/jmv.26846","article-title":"Droplet Digital PCR of Viral DNA\/RNA, Current Progress, Challenges, and Future Perspectives","volume":"93","author":"Kojabad","year":"2021","journal-title":"J. Med. Virol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"BSR20181170","DOI":"10.1042\/BSR20181170","article-title":"Application of Droplet Digital PCR to Detect the Pathogens of Infectious Diseases","volume":"38","author":"Li","year":"2018","journal-title":"Biosci. Rep."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.tube.2019.07.001","article-title":"Droplet Digital PCR Applications in the Tuberculosis World","volume":"117","author":"Nyaruaba","year":"2019","journal-title":"Tuberculosis"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1038\/s41598-020-80715-1","article-title":"Digital Droplet PCR Accurately Quantifies SARS-CoV-2 Viral Load from Crude Lysate without Nucleic Acid Purification","volume":"11","author":"Vasudevan","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Morisset, D., \u0160tebih, D., Milavec, M., Gruden, K., and \u017del, J. (2013). Quantitative Analysis of Food and Feed Samples with Droplet Digital PCR. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0062583"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"549","DOI":"10.46234\/ccdcw2020.145","article-title":"A Reemergent Case of Bubonic Plague-Inner Mongolia Autonomous Region, China, July, 2020","volume":"2","author":"Shen","year":"2020","journal-title":"China CDC Wkly."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Wang, P., Shi, L., Zhang, F., Guo, Y., Zhang, Z., Tan, H., Cui, Z., Ding, Y., Liang, Y., and Liang, Y. (2018). Ten Years of Surveillance of the Yulong Plague Focus in China and the Molecular Typing and Source Tracing of the Isolates. PLoS Negl. Trop. Dis., 12.","DOI":"10.1371\/journal.pntd.0006352"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/978-1-4939-9877-7_3","article-title":"Detection, Isolation, and Characterization of Plasmids in the Environment","volume":"2075","author":"Blau","year":"2020","journal-title":"Methods Mol. Biol."},{"key":"ref_32","first-page":"408","article-title":"Dataset of Yunnan soil species based on the second national soil survey","volume":"10","author":"Gao","year":"2025","journal-title":"China Sci. Data (Chin. Engl. Online Version)"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e2209816119","DOI":"10.1073\/pnas.2209816119","article-title":"No Evidence for Persistent Natural Plague Reservoirs in Historical and Modern Europe","volume":"119","author":"Stenseth","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"12682","DOI":"10.1038\/s41598-026-43695-2","article-title":"Land-Use Types Shape Soil Bacterial Communities, Co-Occurrence Networks, and Predicted Functions in Karst Ecosystems","volume":"16","author":"Fang","year":"2026","journal-title":"Sci. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"104595","DOI":"10.1016\/j.still.2020.104595","article-title":"Temporal Changes in Soil Microbial Properties and Nutrient Dynamics under Climate Smart Agriculture Practices","volume":"199","author":"Jat","year":"2020","journal-title":"Soil Tillage Res."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/6\/616\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T10:06:00Z","timestamp":1781085960000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/6\/616"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,9]]},"references-count":35,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6]]}},"alternative-id":["pathogens15060616"],"URL":"https:\/\/doi.org\/10.3390\/pathogens15060616","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,9]]}}}