Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km2) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes—urbanization and forest edge creation—on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new “suites” of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction—including increased greenhouse gas production—in temperate forest regions that are subsumed by urban expansion, both now and in the future.
Tatsumi, Chikae, et al. "Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil." Proceedings of the National Academy of Sciences of the United States of America, vol. 120, no. 36, Aug. 2023. https://doi.org/10.1073/pnas.2307519120
Tatsumi, Chikae, Atherton, Kathryn F., Garvey, Sarah M., Conrad-Rooney, Emma, Morreale, Luca L., Hutyra, Lucy R., Templer, Pamela H., & Bhatnagar, Jennifer M. (2023). Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil. Proceedings of the National Academy of Sciences of the United States of America, 120(36). https://doi.org/10.1073/pnas.2307519120
Tatsumi, Chikae, Atherton, Kathryn F., Garvey, Sarah M., et al., "Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil," Proceedings of the National Academy of Sciences of the United States of America 120, no. 36 (2023), https://doi.org/10.1073/pnas.2307519120
@article{osti_1997283,
author = {Tatsumi, Chikae and Atherton, Kathryn F. and Garvey, Sarah M. and Conrad-Rooney, Emma and Morreale, Luca L. and Hutyra, Lucy R. and Templer, Pamela H. and Bhatnagar, Jennifer M.},
title = {Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil},
annote = {Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km2) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes—urbanization and forest edge creation—on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new “suites” of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction—including increased greenhouse gas production—in temperate forest regions that are subsumed by urban expansion, both now and in the future.},
doi = {10.1073/pnas.2307519120},
url = {https://www.osti.gov/biblio/1997283},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
issn = {ISSN 0027-8424},
number = {36},
volume = {120},
place = {United States},
publisher = {National Academy of Sciences},
year = {2023},
month = {08}}
Boston Univ., MA (United States); Univ. of California, Oakland, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231; SC0020403
OSTI ID:
1997283
Alternate ID(s):
OSTI ID: 2421602 OSTI ID: 2570209
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 36 Vol. 120; ISSN 1091-6490; ISSN 0027-8424