Non-Mycorrhizal Fungal Presence Within Roots Increases Across an Urban Gradient in Berlin, Germany

Symbioses between plants and fungi are important in both promoting plant fitness and maintaining soil structure. The ways in which these relationships change across an urban gradient is subject to debate. Here we measured root colonisation including the presence of arbuscular mycorrhizal fungi, non-mycorrhizal fungi, and root hair presence. We found no evidence of changes in levels of arbuscular mycorrhizal fungal colonisation across an urban gradient, colonisation levels being driven instead by plant community. However, we did observe an increase in non-mycorrhizal fungal colonisation in association with increasing urbanity. Additionally, we observed an urban-related increase in root hair presence. Using principal component analysis we were able to provide strong evidence for these patterns being driven by an “urban syndrome”, rather than soil chemistry. Our findings have important implications for the wider understanding of abiotic stresses on fungal endophyte presence and shed light on the impacts of urbanity upon plant roots.

[1]  M. Rillig,et al.  Soil Physico-Chemical Properties Change Across an Urbanity Gradient in Berlin , 2021, Frontiers in Environmental Science.

[2]  D. Gozdowski,et al.  Effect of salt stress in urban conditions on two Acer species with different sensitivity , 2021, PeerJ.

[3]  I. Kowarik,et al.  CityScapeLab Berlin: A Research Platform for Untangling Urbanization Effects on Biodiversity , 2020 .

[4]  Jens Kattge,et al.  The fungal collaboration gradient dominates the root economics space in plants , 2020, Science Advances.

[5]  M. Hanfi,et al.  Heavy metal contamination in urban surface sediments: sources, distribution, contamination control, and remediation , 2019, Environmental Monitoring and Assessment.

[6]  S. Raza,et al.  Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance , 2019, Front. Plant Sci..

[7]  M. Rillig,et al.  Fungal Traits Important for Soil Aggregation , 2019, bioRxiv.

[8]  C. Leyval,et al.  From Darkness to Light: Emergence of the Mysterious Dark Septate Endophytes in Plant Growth Promotion and Stress Alleviation , 2019, Endophytes for a Growing World.

[9]  M. Rillig,et al.  Visualizing the dynamics of soil aggregation as affected by arbuscular mycorrhizal fungi , 2019, The ISME Journal.

[10]  J. Thioulouse Multivariate Analysis of Ecological Data with ade4 , 2018 .

[11]  D. Sauer,et al.  Urbanization Leads to Increases in pH, Carbonate, and Soil Organic Matter Stocks of Arable Soils of Kumasi, Ghana (West Africa) , 2018, Front. Environ. Sci..

[12]  J. Maciá‐Vicente,et al.  The effects of fungal root endophytes on plant growth are stable along gradients of abiotic habitat conditions , 2018, FEMS microbiology ecology.

[13]  C. Leyval,et al.  Differential growth promotion of poplar and birch inoculated with three dark septate endophytes in two trace element-contaminated soils , 2017, International journal of phytoremediation.

[14]  D. Richardson,et al.  Non-native species in urban environments: patterns, processes, impacts and challenges , 2017, Biological Invasions.

[15]  R. Standish,et al.  Fine root endophytes under scrutiny: a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina , 2017, Mycorrhiza.

[16]  M. Romantschuk,et al.  Soil microbial communities are shaped by vegetation type and park age in cities under cold climate , 2017, Environmental microbiology.

[17]  I. Ibáñez,et al.  Plant-mycorrhizal fungi associations along an urbanization gradient: implications for tree seedling survival , 2017, Urban Ecosystems.

[18]  N. Ferrol,et al.  The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. , 2016, Journal of experimental botany.

[19]  W. Liu,et al.  Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil , 2016, Scientific Reports.

[20]  D. Lang,et al.  A review of urban ecosystem services: six key challenges for future research , 2015 .

[21]  A. Jumpponen,et al.  Mutualism–parasitism paradigm synthesized from results of root-endophyte models , 2015, Front. Microbiol..

[22]  D. Reinhardt,et al.  Phosphorus and Nitrogen Regulate Arbuscular Mycorrhizal Symbiosis in Petunia hybrida , 2014, PloS one.

[23]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[24]  M. Rillig,et al.  Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis , 2013, Plant and Soil.

[25]  Laurent Bonneau,et al.  Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. , 2013, The New phytologist.

[26]  M. Zobel,et al.  Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology. , 2013, Ecology.

[27]  Gan Zhang,et al.  Water infiltration in urban soils and its effects on the quantity and quality of runoff , 2011 .

[28]  J. Klironomos,et al.  The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments , 2011, Mycorrhiza.

[29]  M. McCarthy,et al.  Fungi and the urban environment: A review , 2010 .

[30]  J. Bever,et al.  Mycorrhizal Symbioses and Plant Invasions , 2009 .

[31]  J. Bever,et al.  Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. , 2009, Ecology.

[32]  C. Nilsson,et al.  Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework , 2009 .

[33]  Aura Virginia,et al.  ARBUSCULAR MYCORRHIZAL AND DARK SEPTATE ENDOPHYTIC FUNGI IN URBAN PRESERVES AND SURROUNDING SONORAN DESERT , 2009 .

[34]  M. McKinney,et al.  Effects of urbanization on species richness: A review of plants and animals , 2008, Urban Ecosystems.

[35]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[36]  Christina E. Wells,et al.  SOIL INOCULUM POTENTIAL AND ARBUSCULAR MYCORRHIZAL COLONIZATION OF ACER RUBRUM IN FORESTED AND DEVELOPED LANDSCAPES , 2005 .

[37]  A. Jumpponen,et al.  Seeking the elusive function of the root-colonising dark septate endophytic fungi , 2005 .

[38]  J. Piotrowski,et al.  The effects of arbuscular mycorrhizas on soil aggregation depend on the interaction between plant and fungal species. , 2004, The New phytologist.

[39]  R. Clárk Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH , 1997, Plant and Soil.

[40]  R. Watling Pulling the threads together: habitat diversity , 1997, Biodiversity & Conservation.

[41]  M. Carreiro,et al.  Forest Remnants Along Urban-Rural Gradients: Examining Their Potential for Global Change Research , 2005, Ecosystems.

[42]  C. Gries,et al.  Preliminary assessment of arbuscular mycorrhizal fungal diversity and community structure in an urban ecosystem , 2003, Mycorrhiza.

[43]  L. Ziska,et al.  Cities as harbingers of climate change: common ragweed, urbanization, and public health. , 2003, The Journal of allergy and clinical immunology.

[44]  Gan‐Lin Zhang,et al.  Phosphorus-enriched soils of urban and suburban Nanjing and their effect on groundwater phosphorus , 2001 .

[45]  Y. Dalpé,et al.  Soil pH-induced changes in root colonization, diversity, and reproduction of symbiotic arbuscular mycorrhizal fungi from healthy and declining maple forests , 2000 .

[46]  G. Lovett,et al.  Atmospheric deposition to oak forests along an urban - rural gradient. , 2000 .

[47]  C. Field,et al.  Plant species-specific changes in root-inhabiting fungi in a California annual grassland: responses to elevated CO2 and nutrients , 1998, Oecologia.

[48]  N. Sagara Association of ectomycorrhizal fungi with decomposed animal wastes in forest habitats: a cleaning symbiosis? , 1995 .

[49]  G. Fairchild,et al.  A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. , 1990, The New phytologist.

[50]  X. Xian,et al.  Effect of pH on chemical forms and plant availability of cadmium, zinc, and lead in polluted soils , 1989 .

[51]  K. Boedijn Trypan blue as stain for fungi. , 1956, Stain technology.