Next Article in Journal
Serosurvey of Tick-Borne Encephalitis Virus Infection in Romania
Previous Article in Journal
Genetic Diversification and Resistome of Coagulase-Negative Staphylococci from Nostrils of Healthy Dogs and Dog-Owners in La Rioja, Spain
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 13
Issue 3
10.3390/pathogens13030230
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Prevalence, Diversity, and Virulence of Campylobacter Carried by Migratory Birds at Four Major Habitats in China

by
Shanrui Wu
1,
Ru Jia
2,
Ying Wang
1,
Jie Li
1,
Yisong Li
1,
Lan Wang
1,
Yani Wang
1,
Chao Liu
1,
Elena M. Jia
3,
Yihua Wang
2,
Guogang Zhang
2 and
Jie Liu
1,*
1
School of Public Health, Qingdao University, Qingdao 266073, China
2
Key Laboratory of Biodiversity Conservation of National Forestry and Grassland Administration, Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Bei**g 100091, China
3
School of Science, Hong Kong University of Science and Technology, Hong Kong 999077, China
*
Author to whom correspondence should be addressed.
Pathogens 2024, 13(3), 230; https://doi.org/10.3390/pathogens13030230
Submission received: 15 February 2024 / Revised: 2 March 2024 / Accepted: 4 March 2024 / Published: 6 March 2024
(This article belongs to the Section Bacterial Pathogens)
Browse Figures
Versions Notes

Abstract

:
Campylobacter species, especially C. jejuni and C. coli, are the main zoonotic bacteria causing human gastroenteritis. A variety of Campylobacter species has been reported in wild birds, posing a potential avian–human transmission pathway. Currently, there has been little surveillance data on Campylobacter carriage in migratory birds in China. In the current work, fresh fecal drop**s from individual migratory birds were collected at four bird wintering/stopover sites in China from May 2020 to March 2021. Nucleic acid was extracted and tested for Campylobacter with PCR-based methods. Overall, 73.8% (329/446) of the samples were positive for Campylobacter, demonstrating location and bird host specificity. Further speciation revealed the presence of C. jejuni, C. coli, C. lari, C. volucris, and an uncharacterized species, which all harbored a variety of virulence factors. Phylogenetic analysis performed on concatenated 16S rRNA-atpA-groEL genes elucidated their genetic relationship, demonstrating both inter- and intra-species diversity. The wide distribution and high diversity of Campylobacter spp. detected in migratory birds in China indicated potential transmission across territories. The existence of virulence factors in all of these species highlighted their public health importance and the necessity of monitoring and controlling Campylobacter and other pathogens carried by migratory birds.

1. Introduction

As one of the major global causes of diarrheal diseases, Campylobacter has been considered the most widespread zoonotic agent of human gastroenteritis in the world [1,2]. Campylobacter is also one of the most prevalent pathogens identified from foodborne disease in developed countries, and although epidemiological data are incomplete, Campylobacter infection has been detected to varying degrees in develo** countries [3,4,5,6]. In its estimate of the worldwide burden of foodborne illnesses, the WHO estimated that foodborne Campylobacter spp. caused more than 95 million illnesses, 21,374 deaths, and nearly 2,142,000 DALYs10 in 2010 [7,8]. As is well known, the most prevalent species associated with campylobacteriosis are Campylobacter jejuni and Campylobacter coli. Notably, other Campylobacter species of clinical significance have been identified, including Campylobacter concisus, Campylobacter lari, Campylobacter upsaliensis [6], and Campylobacter ureolyticus [9,10]. In addition to common gastroenteritis, Campylobacter is also associated with a number of immunoreactive complications, such as Guillain-Barre syndrome and Miller-Fisher syndrome, as well as brain abscess, meningitis, bacteremia, septicemia, endocarditis, myocarditis, reactive arthritis, and clinical manifestations leading to reproductive tract complications, which often occur in immunocompromised people, such as the elderly and children [11,12,13].The important and extensive clinical significance of Campylobacter is being increasingly recognized.
Birds, especially migratory birds, have long played an important role in the spatial transmission of zoonosis diseases, e.g., avian flu [14]. Birds can indirectly spread pathogens via feces, by contaminating water, and by carrying ticks, etc. [15,16,17,18,19]. As a typical zoonotic bacterial pathogen, Campylobacter is widely detected and researched in wild and domestic animals, particularly poultry and livestock, such as chicken, pigs, cattle, sheep, and the corresponding food products [20,21,22,23]. A variety of migratory birds have also been found to be excellent vectors and reservoirs of Campylobacter [24,25,26]. There are nine migratory bird migration routes in the world, three of which pass through China. In other words, most of the land in China is on one of these important global bird migration routes [27]. However, little is known about pathogen carriage in the migratory birds in China.
** samples from migratory birds were collected at four bird wintering/stopover sites in China, namely ** collection. For precise identification, the mitochondrial cytochrome oxidase subunit I gene (COI) was amplified with the primers specifically designed for birds [33] with modifications to expand the detection scope to accommodate the bird types in the current study. The amplicons were sequenced.

2.7. Statistical Analyses

A chi-square test or Fisher’s exact probability method was performed to compare the prevalence of Campylobacter detection and the presence of virulence genes between regions or migratory birds. SPSS software, version 26.0, was used for the analysis. Two-tailed p values were calculated, and values of 0.05 were considered statistically significant.

3. Results

3.1. Migratory Bird Types Included in the Current Study

Based on the observation during the sample collection, the bird populations in Heilongjiang, ** samples. The detection in Heilongjiang (41/43, 95.3%) and Hebei (80/87, 92.0%) was higher than that in **s, respectively. In addition, 20.8% (35/168) of the samples were not speciated or indistinguishable among C. novaezeelandiae, C. armoricus, C. peloridis, and C. volucris. C. jejuni/C. coli was mostly detected in **s, respectively. Therefore, it is not surprising that exposure to contaminated wild bird drop**s in playgrounds has been identified as a new environmental source of campylobacteriosis, especially for children [47]. The active long-term surveillance of Campylobacter in wild and domestic animals and the relevant environment is of great importance to understand the transmission pathways and to further provide guidance on cutting down the potential transmission from the wild sources to farms or directly to humans.
Based on the preliminary phylogenetic analysis (Figure 1), Campylobacter jejuni identified in this study clustered with the known isolate from a human source, while all the other species seemed to be closely related to the strains isolated from animal sources. A more vigorous sequence comparison is required to characterize their genetic relationships. Meanwhile, concerning the high prevalence and wide distribution of these Campylobacter species, particularly the uncharacterized RM12651-like species, surveillance in people with potential exposure would be of great significance for determine the clinical or public health relevance. With high sensitivity and specificity, multiplex real-time PCR can be developed based on the current findings and utilized for the quick screening of these Campylobacter species in humans, domestic animals, and the environment.
The main limitation of the current study is that bacterial culture was not feasible because of the use of antibiotics during sample collection and storage as the standard procedure for avian flu studies. Therefore, similar to a large number of studies using molecular methods, which do not discriminate the viability of the pathogens, PCR detection alone may overestimate the potential health risk. Moreover, this has hindered the genomic analysis of the uncharacterized RM12651-like species. Instead, metagenomic sequencing is ongoing with the intention to confirm its relationship with the RM12651 strain. The lack of isolates also prevented us from characterizing the antimicrobial resistance, as it has been cumbersome to interpret the detection of ARGs in complexed specimens [29]. However, we were able to interrogate the Campylobacter-specific AMR targets associated with fluoroquinolone and macrolide resistance, respectively. Fluoroquinolones, aminoglycosides, and macrolides are the most commonly used drugs for the treatment of human campylobacteriosis. These antibiotics are also frequently applied to food animals, such as poultry, to control bacterial infections on farms to improve the animals’ growth [32,48,49]. The potential role of migratory birds in the transfer of antibiotic resistance genes and antibiotic-resistant bacteria has gradually attracted attention [50,51,52,53], including drug resistant Campylobacter. Another limitation was that temporal variation and seasonality of Campylobacter carriage by migratory birds were not evaluated due to the availability of the samples. Studies have shown the detection of certain pathogens associated with the seasonal migration of wild birds or animals, such as highly pathogenic avian influenza H5N8 [40] and Kyasanur forest disease virus [54]. Such information would improve the targeted prevention and control of diseases.
A further assessment and investigation of health risks resulting from the carriage of Campylobacter, in particular emerging species, and other pathogens by migratory birds is needed. Once confirmed, appropriate measures, such as plant-mediated biofilters [55], may be taken to attenuate these bacteria in the corresponding environments with a one health approach.

Supplementary Materials

The following supporting information can be downloaded at: https://mdpi.longhoe.net/article/10.3390/pathogens13030230/s1, Table S1: Primer sequences used in this study [2,29,31,32,36,56,57]; Table S2: Distribution of Campylobacter detected in different migratory bird species at the four habitats; Table S3: Detection of virulence genes in the five Campylobacter species; Table S4: Presumptive RM12651 virulence genes identified by BLAST analysis of protein sequences. Subject sequences are predominantly from C. jejuni, C. coli, C. lari, and C. volucris (see Materials and Methods); Table S5: Presumptive RM12651 virulence genes shared with C. jejuni, C. coli, C. lari, and C. volucris; Table S6: Presumptive RM12651 virulence genes unique to C. jejuni, C. coli, C. lari, and C. volucris; Figure S1: Phylogenetic analysis based on the 16S rRNA gene in different habitats and migratory birds.

Author Contributions

Conceptualization, J.L. (Jie Liu) and G.Z.; methodology, S.W., R.J., J.L. (Jie Li), Y.L. and L.W.; Software, Y.L.; validation, S.W.; formal analysis, S.W. and J.L. (Jie Liu); investigation, S.W., R.J., Y.W. (Ying Wang), J.L. (Jie Li), L.W., Y.W. (Yani Wang), C.L., E.M.J. and Y.W. (Yihua Wang); resources, G.Z. and Y.W. (Yihua Wang); data curation, S.W. and J.L. (Jie Liu); writing—original draft preparation, S.W. and J.L. (Jie Liu); writing—review and editing, S.W., R.J., Y.W. (Ying Wang), J.L. (Jie Li), Y.L., L.W., Y.W. (Yani Wang), C.L., E.M.J., Y.W. (Yihua Wang), G.Z. and J.L. (Jie Liu); supervision, J.L. (Jie Liu); project administration, J.L. (Jie Liu); funding acquisition, G.Z. and J.L. (Jie Liu). All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (No. 32070530 to G.Z.), National Key Research and Development Program of China (No. 2021YFC0863400 to J.L. (Jie Liu)), and National Natural Science Foundation for Youth (No. 32100002 to Y.L.).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The sequences generated and presented in this study have been deposited in NCBI GenBank, with the accession numbers PP333242 through PP333389 assigned. The information for the sequences used for virulence factor prediction is presented in the Supplementary Material. The raw data are available upon request from the corresponding author.

Acknowledgments

The authors would like to thank Yuxin Zheng from Qingdao University, China, for his valuable guidance and support, the staff from the Chinese Academy of Forestry that were involved in fecal sample collection and transportation, and HuanWan Testing Consulting Co., Ltd., Qingdao, China, for assisting with sample treatment.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Campylobacter. Available online: https://www.who.int/zh/news-room/fact-sheets/detail/campylobacter (accessed on 3 February 2024).
  2. Liu, J.; Platts-Mills, J.A.; Juma, J.; Kabir, F.; Nkeze, J.; Okoi, C.; Operario, D.J.; Uddin, J.; Ahmed, S.; Alonso, P.L.; et al. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: A reanalysis of the GEMS case-control study. Lancet 2016, 388, 1291–1301. [Google Scholar] [CrossRef]
  3. Kaakoush, N.O.; Castaño-Rodríguez, N.; Mitchell, H.M.; Man, S.I.M. Global Epidemiology of Campylobacter Infection. Clin. Microbiol. Rev. 2015, 28, 687–720. [Google Scholar] [CrossRef]
  4. Tack, D.M.; Marder, E.P.; Griffin, P.M.; Cieslak, P.R.; Dunn, J.; Hurd, S.; Scallan, E.; Lathrop, S.; Muse, A.; Ryan, P.; et al. Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2015–2018. Morb. Mortal. Wkly. Rep. 2019, 68, 369–373. [Google Scholar] [CrossRef] [PubMed]
  5. Joensen, K.G.; Schjørring, S.; Gantzhorn, M.R.; Vester, C.T.; Nielsen, H.L.; Engberg, J.H.; Holt, H.M.; Ethelberg, S.; Müller, L.; Sandø, G.; et al. Whole genome sequencing data used for surveillance of Campylobacter infections: Detection of a large continuous outbreak, Denmark, 2019. Euro Surveill. 2021, 26, 2001396. [Google Scholar] [CrossRef] [PubMed]
  6. Lakhan, C.; Badrie, N.; Ramsubhag, A.; Indar, L. Detection of Foodborne Pathogens in Acute Gastroenteritis Patient’s Stool Samples Using the BioFire® FilmArray® Gastrointestinal PCR Panel in the Republic of Trinidad and Tobago, West Indies. Microorganisms 2022, 10, 1601. [Google Scholar] [CrossRef] [PubMed]
  7. Zhou, K.; Hasegawa, A. Call for Experts on the Microbiological Risk Assessment of Non-Typhoidal Salmonella spp. and Campylobacter spp. in Poultry Meat. Available online: https://www.who.int/news-room/articles-detail/call-for-experts-on-the-microbiological-risk-assessment-of-non-typhoidal-salmonella-spp.-and-campylobacter-spp.-in-poultry-meat (accessed on 14 September 2023).
  8. WHO. WHO Estimates of the Global Burden of Foodborne Diseases Foodborne Diseases Burden Epidemiology Reference Group 2007–2015. Available online: https://www.who.int/publications/i/item/9789241565165 (accessed on 14 September 2023).
  9. Silva, W.C.; Targino, B.N.; Gonçalves, A.G.; Silva, M.R.; Hungaro, H.M. Chapter 13-Campylobacter: An Important Food Safety Issue. In Food Safety and Preservation: Modern Biological Approaches to Improving Consumer Health; Grumezescu, A.M., Holban, A.M., Eds.; Academic Press: Cambridge, MA, USA, 2018; pp. 391–430. [Google Scholar]
  10. Man, S.M. The clinical importance of emerging Campylobacter species. Nat. Rev. Gastroenterol. Hepatol. 2011, 8, 669–685. [Google Scholar] [CrossRef]
  11. Ngobese, B.; Zishiri, O.T.; El Zowalaty, M.E. Molecular detection of virulence genes in Campylobacter species isolated from livestock production systems in South Africa. J. Integr. Agric. 2020, 19, 1656–1670. [Google Scholar] [CrossRef]
  12. Costa, D.; Iraola, G. Pathogenomics of Emerging Campylobacter Species. Clin. Microbiol. Rev. 2019, 32, 100–128. [Google Scholar] [CrossRef] [PubMed]
  13. van den Berg, B.; Walgaard, C.; Drenthen, J.; Fokke, C.; Jacobs, B.C.; van Doorn, P.A. Guillain-Barre syndrome: Pathogenesis, diagnosis, treatment and prognosis. Nat. Rev. Neurol. 2014, 10, 469–482. [Google Scholar] [CrossRef] [PubMed]
  14. Tsiodras, S.; Kelesidis, T.; Kelesidis, I.; Bauchinger, U.; Falagas, M.E. Human infections associated with wild birds. J. Infect. 2008, 56, 83–98. [Google Scholar] [CrossRef]
  15. Wang, D.; Li, M.; ** system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J. Clin. Microbiol. 2005, 43, 2315–2329. [Google Scholar] [CrossRef]
  16. Dingle, K.E.; Colles, F.M.; Wareing, D.R.; Ure, R.; Fox, A.J.; Bolton, F.E.; Bootsma, H.J.; Willems, R.J.; Urwin, R.; Maiden, M.C. Multilocus sequence ty** system for Campylobacter jejuni. J. Clin. Microbiol. 2001, 39, 14–23. [Google Scholar] [CrossRef]
  17. Poudel, S.; Li, T.; Chen, S.; Zhang, X.; Cheng, W.H.; Sukumaran, A.T.; Kiess, A.S.; Zhang, L. Prevalence, Antimicrobial Resistance, and Molecular Characterization of Campylobacter Isolated from Broilers and Broiler Meat Raised without Antibiotics. Microbiol. Spectr. 2022, 10, e0025122. [Google Scholar] [CrossRef] [PubMed]
  18. de Melo, A.A.; Nunes, R.; Telles, M.P.d.C. Same information, new applications: Revisiting primers for the avian COI gene and improving DNA barcoding identification. Org. Divers. Evol. 2021, 21, 599–614. [Google Scholar] [CrossRef]
  19. Rossler, E.; Olivero, C.; Soto, L.P.; Frizzo, L.S.; Zimmermann, J.; Rosmini, M.R.; Sequeira, G.J.; Signorini, M.L.; Zbrun, M.V. Prevalence, genotypic diversity and detection of virulence genes in thermotolerant Campylobacter at different stages of the poultry meat supply chain. Int. J. Food Microbiol. 2020, 326, 108641. [Google Scholar] [CrossRef] [PubMed]
  20. Wei, B.; Kang, M.; Jang, H.K. Genetic characterization and epidemiological implications of Campylobacter isolates from wild birds in South Korea. Transbound. Emerg. Dis. 2019, 66, 56–65. [Google Scholar] [CrossRef]
  21. Miller, W.G.; Yee, E.; Jolley, K.A.; Chapman, M.H. Use of an improved atpA amplification and sequencing method to identify members of the Campylobacteraceae and Helicobacteraceae. Lett. Appl. Microbiol. 2014, 58, 582–590. [Google Scholar] [CrossRef] [PubMed]
  22. Konkel, M.E.; Talukdar, P.K.; Negretti, N.M.; Klappenbach, C.M. Taking Control: Campylobacter jejuni Binding to Fibronectin Sets the Stage for Cellular Adherence and Invasion. Front. Microbiol. 2020, 11, 564. [Google Scholar] [CrossRef]
  23. Bolton, D.J. Campylobacter virulence and survival factors. Food Microbiol. 2015, 48, 99–108. [Google Scholar] [CrossRef] [PubMed]
  24. Young, K.T.; Davis, L.M.; Dirita, V.J. Campylobacter jejuni: Molecular biology and pathogenesis. Nat. Rev. Microbiol. 2007, 5, 665–679. [Google Scholar] [CrossRef] [PubMed]
  25. Zhang, G.G.; Li, B.Y.; Raghwani, J.; Vrancken, B.; Jia, R.; Hill, S.C.; Fournie, G.; Cheng, Y.C.; Yang, Q.Q.; Wang, Y.X.; et al. Bidirectional Movement of Emerging H5N8 Avian Influenza Viruses Between Europe and Asia via Migratory Birds Since Early 2020. Mol. Biol. Evol. 2023, 40, msad019. [Google Scholar] [CrossRef] [PubMed]
  26. Liu, D.; Zhang, G.; Li, F.; Ma, T.; Lu, J.; Qian, F. A revised species population estimate for the Bar-headed Goose (Anser indicus). Avian Res. 2017, 8, 7. [Google Scholar] [CrossRef]
  27. Zhang, J.; **e, Y.; Li, L.; Batbayar, N.; Deng, X.; Damba, I.; Meng, F.; Cao, L.; Fox, A.D. Assessing site-safeguard effectiveness and habitat preferences of Bar-headed Geese (Anser indicus) at their stopover sites within the Qinghai-Tibet Plateau using GPS/GSM telemetry. Avian Res. 2020, 11, 1–13. [Google Scholar] [CrossRef]
  28. Zhou, X.; Li, J.; Yang, H.; Zhang, X.; Wang, M.; Cao, S. Study on the Potential of World Natural Heritage in **ngkai Hu Nature Reserve, Heilongjiang Province. Nat. Herit. 2022, 7, 62–72. [Google Scholar] [CrossRef]
  29. Hua**, L.; Lu, W. Study on Waterbird Diversity by Season in **ngkai Lake National Nature Reserve, Heilongjiang Province, China. Chin. J. Wildl. 2016, 37, 221–227. [Google Scholar] [CrossRef]
  30. Fan, Y.; Zhou, L.; Cheng, L.; Song, Y.; Xu, W. Foraging behavior of the Greater White-fronted Goose (Anser albifrons) wintering at Sheng** Lake: Diet shifts and habitat use. Avian Res. 2020, 11, 1–9. [Google Scholar] [CrossRef]
  31. Jarma, D.; Sánchez, M.I.; Green, A.J.; Peralta-Sánchez, J.M.; Hortas, F.; Sánchez-Melsió, A.; Borrego, C.M. Faecal microbiota and antibiotic resistance genes in migratory waterbirds with contrasting habitat use. Sci. Total Environ. 2021, 783, 146872. [Google Scholar] [CrossRef] [PubMed]
  32. French, N.P.; Midwinter, A.; Holland, B.; Collins-Emerson, J.; Pattison, R.; Colles, F.; Carter, P. Molecular epidemiology of Campylobacter jejuni isolates from wild-bird fecal material in children’s playgrounds. Appl. Environ. Microbiol. 2009, 75, 779–783. [Google Scholar] [CrossRef] [PubMed]
  33. Wieczorek, K.; Osek, J. Antimicrobial resistance mechanisms among Campylobacter. Biomed. Res. Int. 2013, 2013, 340605. [Google Scholar] [CrossRef] [PubMed]
  34. Dai, L.; Sahin, O.; Grover, M.; Zhang, Q. New and alternative strategies for the prevention, control, and treatment of antibiotic-resistant Campylobacter. Transl. Res. 2020, 223, 76–88. [Google Scholar] [CrossRef]
  35. Liakopoulos, A.; Mevius, D.J.; Olsen, B.; Bonnedahl, J. The colistin resistance mcr-1 gene is going wild. J. Antimicrob. Chemother. 2016, 71, 2335–2336. [Google Scholar] [CrossRef]
  36. Mohsin, M.; Raza, S.; Roschanski, N.; Schaufler, K.; Guenther, S. First description of plasmid-mediated colistin-resistant extended-spectrum beta-lactamase-producing Escherichia coli in a wild migratory bird from Asia. Int. J. Antimicrob. Agents 2016, 48, 463–464. [Google Scholar] [CrossRef]
  37. Lin, Y.; Dong, X.; Wu, J.; Rao, D.; Zhang, L.; Faraj, Y.; Yang, K. Metadata Analysis of mcr-1-Bearing Plasmids Inspired by the Sequencing Evidence for Horizontal Transfer of Antibiotic Resistance Genes between Polluted River and Wild Birds. Front. Microbiol. 2020, 11, 352. [Google Scholar] [CrossRef] [PubMed]
  38. Lin, Y.; Dong, X.; Sun, R.; Wu, J.; Tian, L.; Rao, D.; Zhang, L.; Yang, K. Migratory birds-one major source of environmental antibiotic resistance around Qinghai Lake, China. Sci. Total Environ. 2020, 739, 139758. [Google Scholar] [CrossRef]
  39. Singh, B.B.; Gajadhar, A.A. Role of India’s wildlife in the emergence and re-emergence of zoonotic pathogens, risk factors and public health implications. Acta Trop. 2014, 138, 67–77. [Google Scholar] [CrossRef]
  40. Galbraith, P.; Henry, R.; McCarthy, D.T. Plants release, pathogens decease: Plants with documented antimicrobial activity are associated with Campylobacter and faecal indicator attenuation in stormwater biofilters. Sci. Total Environ. 2024, 906, 167474. [Google Scholar] [CrossRef] [PubMed]
  41. Linton, D.; Owen, R.J.; Stanley, J. Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Res. Microbiol. 1996, 147, 707–718. [Google Scholar] [CrossRef] [PubMed]
  42. Hill, J.E.; Paccagnella, A.; Law, K.; Melito, P.L.; Woodward, D.L.; Price, L.; Leung, A.H.; Ng, L.K.; Hemmingsen, S.M.; Goh, S.H. Identification of Campylobacter spp. and discrimination from Helicobacter and Arcobacter spp. by direct sequencing of PCR-amplified cpn60 sequences and comparison to cpnDB, a chaperonin reference sequence database. J. Med. Microbiol. 2006, 55, 393–399. [Google Scholar] [CrossRef] [PubMed]
Pathogens 13 00230 g001
Figure 1. Phylogenetic analysis based on the 16S rRNA—atpA—groEL gene in different habitats and migratory birds. Fasttree was used to construct the tree. Helicobacter was used as an outgroup. The figure was prepared with iTOL (Interactive Tree of Life). Different colors in the two columns represent different regions and birds, respectively. The Bootstrap value is displayed only when it was <0.7.
Figure 1. Phylogenetic analysis based on the 16S rRNA—atpA—groEL gene in different habitats and migratory birds. Fasttree was used to construct the tree. Helicobacter was used as an outgroup. The figure was prepared with iTOL (Interactive Tree of Life). Different colors in the two columns represent different regions and birds, respectively. The Bootstrap value is displayed only when it was <0.7.
Pathogens 13 00230 g001
Pathogens 13 00230 g002
Figure 2. Upset of Campylobacter (C. jejuni, C. coli, C. lari, C. volucris) with respect to the detection of different virulence genes.
Figure 2. Upset of Campylobacter (C. jejuni, C. coli, C. lari, C. volucris) with respect to the detection of different virulence genes.
Pathogens 13 00230 g002
Pathogens 13 00230 g003
Figure 3. Virulence genes detected in RM12651-like Campylobacter sp. (a) Prevalence of virulence-associated genes predicted from the Campylobacter Sp. RM12651 genome at the three sites. ** means p < 0.05; *** means p < 0.005. Hebei was not shown due to the small sample size of RM12651-like Campylobacter. (b) Venn diagram of the distribution of the virulence genes.
Figure 3. Virulence genes detected in RM12651-like Campylobacter sp. (a) Prevalence of virulence-associated genes predicted from the Campylobacter Sp. RM12651 genome at the three sites. ** means p < 0.05; *** means p < 0.005. Hebei was not shown due to the small sample size of RM12651-like Campylobacter. (b) Venn diagram of the distribution of the virulence genes.
Pathogens 13 00230 g003
Table 1. Distribution of Campylobacter species at the four habitat sites.
Table 1. Distribution of Campylobacter species at the four habitat sites.
Campylobacter SpeciesDetection Rate16S IdentityRegion
**zang (n = 82)Qinghai (n = 14)Heilongjiang (n = 25)Hebei (n = 47)
Campylobacter sp. (RM12651)94 (56.0%)100.0 (100.0, 100.0)5114218
C. jejuni #22 (13.1%)100.0 (99.8–100.0)19-12
C. coli #3 (1.8%)100.0 (NA)3---
C. lari13 (7.7%)100.0 (99.8–100.0)3--10
C. volucris5 (3.0%)100.0 (99.8–100.0)1--4
C. novaezeelandiae/armoricus/peloridis/volucris *8 (4.8%)100.0 (99.7–100.0)---8
Uncultured bacterium clone *17 (10.1%)99.6 (97.3–100.0)4 13
Others10 (6.0%)97.5 (96.6–98.2)5 32
* Indistinguishable with 16S rRNA, atpA, or groEL sequencing. # One C. coli isolate was mixed with Campylobacter sp. (RM12651); three C. jejuni isolates were mixed with Campylobacter sp. (RM12651). NA: Not applicable.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Wu, S.; Jia, R.; Wang, Y.; Li, J.; Li, Y.; Wang, L.; Wang, Y.; Liu, C.; Jia, E.M.; Wang, Y.; et al. Prevalence, Diversity, and Virulence of Campylobacter Carried by Migratory Birds at Four Major Habitats in China. Pathogens 2024, 13, 230. https://doi.org/10.3390/pathogens13030230

AMA Style

Wu S, Jia R, Wang Y, Li J, Li Y, Wang L, Wang Y, Liu C, Jia EM, Wang Y, et al. Prevalence, Diversity, and Virulence of Campylobacter Carried by Migratory Birds at Four Major Habitats in China. Pathogens. 2024; 13(3):230. https://doi.org/10.3390/pathogens13030230

Chicago/Turabian Style

Wu, Shanrui, Ru Jia, Ying Wang, Jie Li, Yisong Li, Lan Wang, Yani Wang, Chao Liu, Elena M. Jia, Yihua Wang, and et al. 2024. "Prevalence, Diversity, and Virulence of Campylobacter Carried by Migratory Birds at Four Major Habitats in China" Pathogens 13, no. 3: 230. https://doi.org/10.3390/pathogens13030230

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop