Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Impact of socioeconomic factors on soil-borne animal pathogenic fungi in urban greenspaces

Nature Cities (2024)Cite this article

Subjects

Abstract

Animal pathogenic fungi, including human pathogenic fungi, cause millions of deaths annually. We know that these organisms can be found in our urban greenspaces where we enter in contact with them, yet the contribution of socioeconomic development in shaping the distribution of soil-borne animal pathogens from local to global scales remains virtually unknown. Here we used information from a global survey including 56 cities and a high-resolution local survey within Shanghai and found that socioeconomic factors were crucial in predicting the community composition and diversity of soil-borne pathogens. Our results were consistent after accounting for the effects of climate and soil properties. Trichosporon was identified as a universal indicator species for population density at both the global and local scales. Gross domestic product per capita and number of hospital beds were also critical predictors of a limited proportion of Trichosporon in Shanghai. Our study highlights the influence of human activities in shaping the pathogenic microbiome of cities with potential implications for human health, suggesting that poorer and more populated cities are expected to harbor larger proportions of soil-borne animal and human pathogens.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2: Predictors influencing fungal animal pathogens composition in urban greenspaces.
Fig. 3: Relationships between population density and the diversity of fungal animal pathogens.
Fig. 4: Dominant fungal animal pathogens significantly associated with socioeconomic factors.
Fig. 5: Relationships between Trichosporon abundance and socioeconomic factors in urban greenspaces at local scale.

Similar content being viewed by others

Data availability

The data in this Article are publicly available on figshare33. Further details on the data can be obtained by emailing the corresponding author.

Code availability

The code that supports the findings of this study is available from the corresponding authors upon request.

References

  1. Sun, S. et al. Fungal pathogens. Curr. Biol. 30, 1163–1169 (2020).

    Article  Google Scholar 

  2. Brown, G. D. et al. Hidden killers: human fungal infections. Sci. Transl. Med. 4, 165rv13 (2012).

    Article  Google Scholar 

  3. Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).

    Article  Google Scholar 

  4. Delgado-Baquerizo, M. et al. Global homogenization of the structure and function in the soil microbiome of urban greenspaces. Sci. Adv. 7, eabg5809 (2021).

    Article  Google Scholar 

  5. Tosam, M. J. et al. Global emerging pathogens, poverty and vulnerability: an ethical analysis. Socio-cultural Dimensions of Emerging Infectious Diseases in Africa 20, 243–253 (2019).

    Article  Google Scholar 

  6. Luck, G. W. A review of the relationships between human population density and biodiversity. Biol. Rev. 82, 607–645 (2007).

    Article  Google Scholar 

  7. Alegbeleye, O. O. et al. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: a review. Food Microbiol. 73, 177–208 (2018).

    Article  Google Scholar 

  8. Sun, X. et al. Harnessing soil biodiversity to promote human health in cities. Npj Urban Sustain. 3, 5 (2023).

    Article  Google Scholar 

  9. Chagas, T. C. et al. Update on the genus Trichosporon. Mycopathologia 166, 121–132 (2008).

    Article  Google Scholar 

  10. Archer-Dubon, C. et al. Superficial mycotic infections of the foot in a native pediatric population: a pathogenic role for Trichosporon cutaneum? Pediatr. Dermatol. 20, 299–302 (2010).

    Article  Google Scholar 

  11. Padhye, A. A. et al. Trichosporon loubieri infection in a patient with adult polycystic kidney disease. J. Clin. Microbiol. 41, 479–482 (2003).

    Article  Google Scholar 

  12. Walsh, T. J. et al. Infections due to emerging and uncommon medically important fungal pathogens. Clin. Microbiol. Infect. 10, 48–66 (2004).

    Article  Google Scholar 

  13. Shigeko, K. et al. Invasive infection due to Trichosporon cutaneum in patients with hematologic malignancies. Cancer 82, 484–487 (1998).

    Article  Google Scholar 

  14. Cáliz, J. et al. A long-term survey unveils strong seasonal patterns in the airborne microbiome coupled to general and regional atmospheric circulations. Proc. Natl Acad. Sci. USA 115, 12229–12234 (2018).

    Article  Google Scholar 

  15. Barberán, A. et al. Continental-scale distributions of dust-associated bacteria and fungi. Proc. Natl Acad. Sci. USA 112, 5756–5761 (2015).

    Article  Google Scholar 

  16. Di, Q. et al. Air pollution and mortality in the medicare population. N. Engl. J. Med. 377, 1498–1499 (2017).

    Google Scholar 

  17. Rentschler, J. & Leonova, N. Global air pollution exposure and poverty. Nat. Commun. 14, 4432 (2023).

    Article  Google Scholar 

  18. Cheng, W. et al. Geographic distribution of heavy metals and identification of their sources in soils near large, open-pit coal mines using positive matrix factorization. J. Hazard. Mater. 387, 121666 (2020).

    Article  Google Scholar 

  19. Kabala, C. et al. Conversion of soil pH 1:2.5 KCl and 1:2.5 H2O to 1:5 H2O: conclusions for soil management, environmental monitoring, and international soil databases. Pol. J. Environ. Stud. 25, 647–653 (2016).

    Article  Google Scholar 

  20. Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).

    Article  Google Scholar 

  21. Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248 (2016).

    Article  Google Scholar 

  22. Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993).

    Article  Google Scholar 

  23. White, T. J. et al. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. PCR Protocols: A Guide to Methods and Applications 315–322 (Academic Press, 1990).

  24. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996 (2013).

    Article  Google Scholar 

  25. Wang, Q. et al. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    Article  Google Scholar 

  26. Oksanen, J. et al. Vegan: Community Ecology Package. R Package (The Comprehensive R Archive Network, 2019).

  27. R Core Team. R: A Language and Environment for Statistical Computing (Version 3.6.3) (R Foundation for Statistical Computing, 2020).

  28. Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016).

    Article  Google Scholar 

  29. Jing, X. et al. The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nat. Commun. 6, 8159 (2015).

    Article  Google Scholar 

  30. Caceres, M. D. et al. Indicspecies: relationship between species and groups of sites. R package (The Comprehensive R Archive Network, 2023).

  31. Manzoni, S. et al. The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686 (2008).

    Article  Google Scholar 

  32. Muggeo, V. Segmented: an R package to fit regression models with broken-line relationships. R News 8, 20–25 (2008).

    Google Scholar 

  33. Luo, S. H. et al. Impact of socio-economic factors on soil-borne animal pathogenic fungi in urban greenspaces. figshare https://figshare.com/articles/dataset/URBAN_GLOBAL_LOCAL_dataset/24266059 (2023).

Download references

Acknowledgements

Y.F. acknowledges the financial support from National Natural Science Foundation of China (grant no. 42177297). J.H. acknowledges support from Shanghai Finance Special Project (Soil quality monitoring system for typical urban green spaces in Shanghai) and the Scientific Research Foundation of Shanghai Landscaping & City Appearance Administrative Bureau (G200201). M.D.-B. acknowledges support from TED2021-130908B-C41/AEI/10.13039/501100011033/Unión Europea NextGenerationEU/PRTR and from the Spanish Ministry of Science and Innovation for the I+D+i project PID2020-115813RA-I00 funded by MCIN/AEI/10.13039/501100011033.

Author information

Authors and Affiliations

  1. College of Chemical Engineering, Nanjing Forestry University, Nanjing, China

    Shuhong Luo, Ruirui Chen & Youzhi Feng

  2. Shanghai Wildlife and Protected Natural Areas Research Center, Shanghai, China

    Shuhong Luo & Jigang Han

  3. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China

    Shuhong Luo, Ruirui Chen & Youzhi Feng

  4. Key Laboratory of National Forestry and Grassland Administration on Ecological Landscaping of Challenging Urban Sites, National Forestry and Grassland Innovation Alliance on Afforestation and Landscaping of Challenging Urban Sites, Shanghai Academy of Landscape Architecture Science and Planning, Shanghai, China

    Jigang Han

  5. Laboratorio de Biodiversidad y Funcionamiento Ecosistemico, Instituto de Recursos Naturales y Agrobiología de Sevilla, CSIC, Sevilla, Spain

    Manuel Delgado-Baquerizo

  6. School of Resources and Materials, Northeastern University at Qinhuangdao, Qinhuangdao, China

    Weiwei Zhang

  7. Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing, China

    Youzhi Feng

Authors
  1. Shuhong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jigang Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruirui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuel Delgado-Baquerizo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weiwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Youzhi Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.D.-B. and Y.F. developed the original idea and designed the research with discussion with R.C., J.H. and S.L. M.D.-B. and J.H. coordinated all field and laboratory operations. S.L., M.D.-B. and R.C. analyzed data. Field data were collected by M.D.-B., J.H., W.Z and R.C. The manuscript was written by S.L., R.C., J.H., M.D.-B. and Y.F., with contributions from all co-authors.

Corresponding authors

Correspondence to Jigang Han, Ruirui Chen or Manuel Delgado-Baquerizo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Cities thanks Shubo Fang, Ferry Hagen and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4 and Table 1.

Reporting Summary

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, S., Han, J., Chen, R. et al. Impact of socioeconomic factors on soil-borne animal pathogenic fungi in urban greenspaces. Nat Cities (2024). https://doi.org/10.1038/s44284-024-00073-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s44284-024-00073-1

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology