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Enea, M., Beauregard, J., De Bellis, T., Faticov, M. & Laforest-Lapointe, I. (2025). The temperate forest phyllosphere and rhizosphere microbiome: a case study of sugar maple. Frontiers in Microbiology, 15, Article ID 1504444.
Open this publication in new window or tab >>The temperate forest phyllosphere and rhizosphere microbiome: a case study of sugar maple
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2025 (English)In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 15, article id 1504444Article, review/survey (Refereed) Published
Abstract [en]

The interactions between sugar maple (Acer saccharum, Marshall) and its microbial communities are important for tree fitness, growth, and establishment. Despite recent progress in our understanding of the rhizosphere and phyllosphere microbial communities of sugar maple, many outstanding knowledge gaps remain. This review delves into the relationships between sugar maple and its microbes, as climate change alters plant species distributions. It highlights the multifaceted roles of key microbes, such as arbuscular mycorrhizal (AM) fungi and pathogens, in affecting the distribution and establishment of sugar maple in novel habitats. Furthermore, this review examines how microbial communities in different compartments contribute to tree fitness. Finally, it explores how microbial dispersal and altered species interactions under changing environmental conditions can affect sugar maple's ability to migrate beyond its current range, emphasizing the different scenarios associated with such shifts. In the rhizosphere, AM fungi are known for their roles in nutrient acquisition and improving stress tolerance. Yet, key questions remain about how these fungi interact with other microbes, how soil chemistry and climate change alter these interactions, and how the presence of beneficial microbes influences sugar maple's establishment. Additionally, the role of dark septate endophytes (DSE) in sugar maple's fitness remains underexplored, emphasizing the need for more research on their diversity and functions. In the phyllosphere, microbial communities are subject to shifts due to rising global change, with potential impacts on sugar maple's fitness. These changes may influence the tree's resistance to pathogens, tolerance to environmental stress, and overall health. Yet, our understanding of these interactions relies mostly on short-read sequencing methods targeting marker genes (e.g., 16S, ITS, 18S), which often fail to identify microbes at the species level. Limitations in molecular techniques and poor microbial reference databases hinder our ability to fully characterize tree-associated microbial diversity and functions. Future research should thus prioritize advanced molecular tools such as shotgun, hybrid, or long-read sequencing. Controlled experiments are also needed to establish causal links between sugar maple fitness and microbial communities, and to study whether microbial communities change throughout the tree's lifespan.

Keywords
Acer saccharum, sugar maple, tree-microbe interactions, rhizosphere, phyllosphere, arbuscular mycorrhizal fungi, climate change
National Category
Microbiology
Identifiers
urn:nbn:se:su:diva-241363 (URN)10.3389/fmicb.2024.1504444 (DOI)001408194600001 ()2-s2.0-85216190648 (Scopus ID)
Available from: 2025-03-28 Created: 2025-03-28 Last updated: 2025-03-28Bibliographically approved
Faticov, M., Amorim, J. H., Abdelfattah, A., van Dijk, L. J. A., Carvalho, A. C., Laforest-Lapointe, I. & Tack, A. J. M. (2024). Local climate, air quality and leaf litter cover shape foliar fungal communities on an urban tree. Ambio, 53(11), 1673-1685
Open this publication in new window or tab >>Local climate, air quality and leaf litter cover shape foliar fungal communities on an urban tree
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2024 (English)In: Ambio, ISSN 0044-7447, E-ISSN 1654-7209, Vol. 53, no 11, p. 1673-1685Article in journal (Refereed) Published
Abstract [en]

Foliar fungi on urban trees are important for tree health, biodiversity and ecosystem functioning. Yet, we lack insights into how urbanization influences foliar fungal communities. We created detailed maps of Stockholm region’s climate and air quality and characterized foliar fungi from mature oaks (Quercus robur) across climatic, air quality and local habitat gradients. Fungal richness was higher in locations with high growing season relative humidity, and fungal community composition was structured by growing season maximum temperature, NO2 concentration and leaf litter cover. The relative abundance of mycoparasites and endophytes increased with temperature. The relative abundance of pathogens was lowest with high concentrations of NO2 and particulate matter (PM2.5), while saprotrophs increased with leaf litter cover. Our findings show that urbanization influences foliar fungi, providing insights for developing management guidelines to promote tree health, prevent disease outbreaks and maintain biodiversity within urban landscapes.

Keywords
Air quality, Fungal communities, Fungal guilds, Leaf litter cover, Local climate, Urban trees
National Category
Ecology Forest Science
Identifiers
urn:nbn:se:su:diva-235539 (URN)10.1007/s13280-024-02041-4 (DOI)001246399200002 ()2-s2.0-85195842082 (Scopus ID)
Available from: 2024-11-26 Created: 2024-11-26 Last updated: 2024-11-26Bibliographically approved
Hoefle, D., Sommer, M., Wassermann, B., Faticov, M., Serra, D., Berg, G., . . . Abdelfattah, A. (2024). Oak seedling microbiome assembly under climate warming and drought. Environmental Microbiome, 19(1), Article ID 62.
Open this publication in new window or tab >>Oak seedling microbiome assembly under climate warming and drought
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2024 (English)In: Environmental Microbiome, E-ISSN 2524-6372, Vol. 19, no 1, article id 62Article in journal (Refereed) Published
Abstract [en]

Despite that climate change is currently one of the most pervasive challenges, its effects on the plant-associated microbiome is still poorly studied. The aim of this study was to evaluate the impact of the independent and combinatory effect of climate warming and drought on the microbiome assembly of oak from seed to seedling. In a multifactorial experimental set up, acorns were subjected to different temperatures (15 °C, 20 °C, and 25 °C) and soil moisture levels (drought (15%) and control (60%)) from germination until the seedling stage, after which the bacterial and fungal communities associated to the rhizosphere and phyllosphere were characterized by amplicon sequencing and qPCR. The results showed a stronger effect of temperature on fungal than on bacterial diversity and the effect was more pronounced in the phyllosphere. Under drought condition, temperature had a significantly negative effect on phyllosphere fungal diversity. In the rhizosphere, temperature had a significant effect on the fungal community composition which was primarily caused by species turnover. Regardless of temperature, Actinobacteriota was significantly enriched in drought, a group of bacteria known to increase plant drought tolerance. This study provides new insights into the effect of climate change on the plant microbiome in natural ecosystems.

Keywords
Climate change, Microbiome assembly, Phyllosphere, Quercus robur L, Rhizosphere
National Category
Microbiology
Identifiers
urn:nbn:se:su:diva-236976 (URN)10.1186/s40793-024-00602-4 (DOI)001300714400001 ()2-s2.0-85202717024 (Scopus ID)
Available from: 2024-12-10 Created: 2024-12-10 Last updated: 2024-12-10Bibliographically approved
Faticov, M., Abdelfattah, A., Hambäck, P. A., Roslin, T. & Tack, A. J. M. (2023). Different spatial structure of plant-associated fungal communities above- and belowground. Ecology and Evolution, 13(5), Article ID e10065.
Open this publication in new window or tab >>Different spatial structure of plant-associated fungal communities above- and belowground
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2023 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 13, no 5, article id e10065Article in journal (Refereed) Published
Abstract [en]

The distribution and community assembly of above- and belowground microbial communities associated with individual plants remain poorly understood, despite its consequences for plant–microbe interactions and plant health. Depending on how microbial communities are structured, we can expect different effects of the microbial community on the health of individual plants and on ecosystem processes. Importantly, the relative role of different factors will likely differ with the scale examined. Here, we address the driving factors at a landscape level, where each individual unit (oak trees) is accessible to a joint species pool. This allowed to quantify the relative effect of environmental factors and dispersal on the distribution of two types of fungal communities: those associated with the leaves and those associated with the soil of Quercus robur trees in a landscape in southwestern Finland. Within each community type, we compared the role of microclimatic, phenological, and spatial variables, and across community types, we examined the degree of association between the respective communities. Most of the variation in the foliar fungal community was found within trees, whereas soil fungal community composition showed positive spatial autocorrelation up to 50 m. Microclimate, tree phenology, and tree spatial connectivity explained little variation in the foliar and soil fungal communities. Foliar and soil fungal communities differed strongly in community structure, with no significant concordance detected between them. We provide evidence that foliar and soil fungal communities assemble independent of each other and are structured by different ecological processes.

Keywords
community ecology, dispersal, metacommunity, microclimate, phenology, phyllosphere microorganisms, soil microorganisms, spatial ecology
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-218063 (URN)10.1002/ece3.10065 (DOI)000993194500001 ()37223309 (PubMedID)2-s2.0-85160946667 (Scopus ID)
Available from: 2023-07-25 Created: 2023-07-25 Last updated: 2024-01-17Bibliographically approved
Ekholm, A., Faticov, M., Tack, A. J. M. & Roslin, T. (2022). Herbivory in a changing climate-Effects of plant genotype and experimentally induced variation in plant phenology on two summer-active lepidopteran herbivores and one fungal pathogen. Ecology and Evolution, 12(1), Article ID e8495.
Open this publication in new window or tab >>Herbivory in a changing climate-Effects of plant genotype and experimentally induced variation in plant phenology on two summer-active lepidopteran herbivores and one fungal pathogen
2022 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 12, no 1, article id e8495Article in journal (Refereed) Published
Abstract [en]

With climate change, spring warming tends to advance plant leaf-out. While the timing of leaf-out has been shown to affect the quality of leaves for herbivores in spring, it is unclear whether such effects extend to herbivores active in summer. In this study, we first examined how spring and autumn phenology of seven Quercus robur genotypes responded to elevated temperatures in spring. We then tested whether the performance of two summer-active insect herbivores (Orthosia gothica and Polia nebulosa) and infection by a pathogen (Erysiphe alphitoides) were influenced by plant phenology, traits associated with genotype or the interaction between these two. Warm spring temperatures advanced both bud development and leaf senescence in Q. robur. Plants of different genotype differed in terms of both spring and autumn phenology. Plant phenology did not influence the performance of two insect herbivores and a pathogen, while traits associated with oak genotype had an effect on herbivore performance. Weight gain for O. gothica and ingestion for P. nebulosa differed by a factor of 4.38 and 2.23 among genotypes, respectively. Herbivore species active in summer were influenced by traits associated with plant genotype but not by phenology. This suggest that plant attackers active in summer may prove tolerant to shifts in host plant phenology-a pattern contrasting with previously documented effects on plant attackers active in spring and autumn.

Keywords
Climate change, Community ecology, Mismatch, Phenology, Trophic interactions
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-203015 (URN)10.1002/ece3.8495 (DOI)000747845400019 ()35136555 (PubMedID)
Available from: 2022-03-21 Created: 2022-03-21 Last updated: 2024-01-17Bibliographically approved
Faticov, M., Desprez-Loustau, M.-L., Kiss, L., Massot, M., Faivre d'Arcier, J., Mutz, J., . . . Tack, A. J. M. (2022). Niche differentiation within a cryptic pathogen complex: climatic drivers and hyperparasitism at multiple spatial scales. Ecography, 2022(2), Article ID e06062.
Open this publication in new window or tab >>Niche differentiation within a cryptic pathogen complex: climatic drivers and hyperparasitism at multiple spatial scales
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2022 (English)In: Ecography, ISSN 0906-7590, E-ISSN 1600-0587, Vol. 2022, no 2, article id e06062Article in journal (Refereed) Published
Abstract [en]

Pathogens are embedded in multi-trophic food webs, which often include co-occurring cryptic species within the same pathogen complex. Nonetheless, we still lack an understanding of what dimensions of the ecological niche might allow these cryptic species to coexist. We explored the role of climate, host characteristics (tree autumn phenology) and attack by the fungal hyperparasite Ampelomyces (a group of fungi attacking plant pathogens) in defining the niches of three powdery mildew species (Erysiphe alphitoidesE. hypophylla and E. quercicola) within a cryptic pathogen complex on the pedunculate oak Quercus robur at the continental (Europe), national (Sweden and France) and landscape scales (a 5 km2 island in southwestern Finland). Previous studies have shown that climate separated the niches of three powdery mildew species (E. alphitoidesE. hypophylla and E. quercicola) in Europe and two species (E. alphitoides and E. quercicola) in France. In our study, we did not detect a significant relationship between temperature or precipitation and the distribution of E. alphitoides and E. hypophylla present in Sweden, while at the landscape scale, temperature, but not relative humidity, negatively affected disease incidence of E. alphitoides in an exceptionally warm year. Tree variation in autumn phenology did not influence disease incidence of powdery mildew species, and hyperparasite presence did not differ among powdery mildew species at the continental, national and landscape scale. Climate did not affect the distribution of the hyperparasite at the continental scale and at the national scale in Sweden. However, climate affected the hyperparasite distribution in France, with a negative relationship between non-growing season temperature and presence of the hyperparasite. Overall, our findings, in combination with earlier evidence, suggest that climatic factors are more important than species interactions in defining the niches of cryptic species within a pathogen complex on oak.

Keywords
climate variation, cryptic pathogen species, hyperparasite, niche differentiation, spatial distribution
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-201879 (URN)10.1111/ecog.06062 (DOI)000743333600001 ()
Available from: 2022-02-10 Created: 2022-02-10 Last updated: 2022-02-10Bibliographically approved
van Dijk, L. J. A., Moreira, X., Barr, A. E., Abdala-Roberts, L., Castagneyrol, B., Faticov, M., . . . Tack, A. J. M. (2022). Urbanization affects oak–pathogen interactions across spatial scales. Ecography, 2022(1), Article ID e06091.
Open this publication in new window or tab >>Urbanization affects oak–pathogen interactions across spatial scales
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2022 (English)In: Ecography, ISSN 0906-7590, E-ISSN 1600-0587, Vol. 2022, no 1, article id e06091Article in journal (Refereed) Published
Abstract [en]

The world is rapidly urbanizing, thereby transforming natural landscapes and changing the abundance and distribution of organisms. However, insights into the effects of urbanization on species interactions, and plant–pathogen interactions in particular, are lacking. We investigated the effects of urbanization on powdery mildew infection on Quercus robur at continental and within-city scales. At the continental scale, we compared infection levels between urban and rural areas of different-sized cities in Europe, and investigated whether plant traits, climatic variables and CO2 emissions mediated the effect of urbanization on infection levels. Within one large city (Stockholm, Sweden), we further explored whether local habitat features and spatial connectivity influenced infection levels during multiple years. At the continental scale, infection severity was consistently higher on trees in urban than rural areas, with some indication that temperature mediated this effect. Within Stockholm city, temperature had no effect, while local accumulation of leaf litter negatively affected powdery mildew incidence in one out of three years, and more connected trees had lower infection levels. This study is the first to describe the effects of urbanization on plant–pathogen interactions both within and among cities, and to uncover the potential mechanisms behind the observed patterns at each scale. 

Keywords
connectivity, local habitat quality, oak powdery mildew, phenolic compounds, plant-pathogen interactions, Quercus robur
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-200551 (URN)10.1111/ecog.06091 (DOI)000729424600001 ()
Available from: 2022-01-07 Created: 2022-01-07 Last updated: 2022-02-24Bibliographically approved
Faticov, M., Abdelfattah, A., Roslin, T., Vacher, C., Hambäck, P., Blanchet, F. G., . . . Tack, A. J. M. (2021). Climate warming dominates over plant genotype in shaping the seasonal trajectory of foliar fungal communities on oak. New Phytologist, 231(5), 1770-1783
Open this publication in new window or tab >>Climate warming dominates over plant genotype in shaping the seasonal trajectory of foliar fungal communities on oak
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2021 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 231, no 5, p. 1770-1783Article in journal (Refereed) Published
Abstract [en]

Leaves interact with a wealth of microorganisms. Among these, fungi are highly diverse and are known to contribute to plant health, leaf senescence and early decomposition. However, patterns and drivers of the seasonal dynamics of foliar fungal communities are poorly understood. We used a multifactorial experiment to investigate the influence of warming and tree genotype on the foliar fungal community on the pedunculate oak Quercus robur across one growing season. Fungal species richness increased, evenness tended to decrease, and community composition strongly shifted during the growing season. Yeasts increased in relative abundance as the season progressed, while putative fungal pathogens decreased. Warming decreased species richness, reduced evenness and changed community composition, especially at the end of the growing season. Warming also negatively affected putative fungal pathogens. We only detected a minor imprint of tree genotype and warming x genotype interactions on species richness and community composition. Overall, our findings demonstrate that warming plays a larger role than plant genotype in shaping the seasonal dynamics of the foliar fungal community on oak. These warming-induced shifts in the foliar fungal community may have a pronounced impact on plant health, plant-fungal interactions and ecosystem functions.

Keywords
climate warming, community composition, foliar fungal community, host genotype, Quercus robur, seasonal dynamics, warming x genotype interaction
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-195822 (URN)10.1111/nph.17434 (DOI)000662923400001 ()33960441 (PubMedID)
Available from: 2021-08-31 Created: 2021-08-31 Last updated: 2022-02-25Bibliographically approved
Ekholm, A., Faticov, M., Tack, A. J. M., Berger, J., Stone, G. N., Vesterinen, E. & Roslin, T. (2021). Community phenology of insects on oak: local differentiation along a climatic gradient. Ecosphere, 12(11), Article ID e03785.
Open this publication in new window or tab >>Community phenology of insects on oak: local differentiation along a climatic gradient
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2021 (English)In: Ecosphere, ISSN 2150-8925, E-ISSN 2150-8925, Vol. 12, no 11, article id e03785Article in journal (Refereed) Published
Abstract [en]

Climate change is advancing the onset of phenological events, with the rate of advance varying among species and trophic levels. In addition, local populations of the same species may show genetic differences in their response to seasonal cues. If populations of interacting species differ in their response, then climate change may result in geographically varying shifts in the community-level distribution of interaction strength. We explored the magnitude of trophic- and species-level responses to temperature in a tritrophic system comprising pedunculate oak, insect herbivores, and their associated parasitoids. We sampled local realizations of this community at five sites along a transect spanning fifteen degrees of latitude. Samples from each trophic level at each site were exposed to the same set of five climatic regimes during overwintering in climate chambers. We then recorded the number of days and degree-days required for oak acorns to develop and insects to emerge. In terms of dates of events, phenology differed among populations. In terms of degree-days, we found that for two species pairs, the heat sum required to develop in spring differed by an additional ∼500 degree-days between trophic levels when overwintering at the highest temperature. For three species, within-population variation in the number of degree-days required for emergence was higher at warmer temperatures. Our findings suggest that changing temperatures can modify interactions within a community by altering the relative phenology of interacting species and that some interactions are more vulnerable than others to a shift in temperature. The geographic variation in the phenological response of a species suggests that there is a genetic component in determining the phenology of local populations. Such local variation blended with interspecific differences in responses makes it complex to understand how communities will respond to warmer temperatures. 

Keywords
climate change, community ecology, mismatch, phenology
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-199538 (URN)10.1002/ecs2.3785 (DOI)000723142700045 ()
Available from: 2021-12-14 Created: 2021-12-14 Last updated: 2022-02-25Bibliographically approved
Faticov, M. (2021). Spatial and temporal ecology of oak-associated fungal communities. (Doctoral dissertation). Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University
Open this publication in new window or tab >>Spatial and temporal ecology of oak-associated fungal communities
2021 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Plants host a large diversity of microorganisms, which includes fungi, bacteria and archaea. Among these, fungi are highly diverse, and known to play a vital role in plant health and in regulation of the essential ecosystem functions. Nevertheless, we still lack a comprehensive understanding of the forces structuring plant-associated fungal communities in space and time. 

The main aim of this thesis was to decipher the drivers of the spatial patterns and temporal dynamics of fungal communities on plants. To this aim, I focused on Quercus robur and its associated fungi. Using a combination of observational and experimental studies, I assessed i) the distribution and drivers of the above- and belowground fungal communities at the landscape scale; ii) the role of climatic and trophic factors in defining the niches of cryptic species within a pathogen complex on oak and iii) the relative importance of warming, plant genotype and their interaction in shaping oak phenology and the seasonal dynamics of the associated fungal and insect communities.

I found that aboveground fungal communities were highly variable among leaves within a single tree, and that belowground fungal communities had a stronger spatial structure than aboveground fungi at the landscape scale. Yet, climate, tree phenology or the distribution of the host tree did not explain spatial patterns in the above- and belowground communities. When focusing on three cryptic powdery mildew species within a pathogen complex on oak, I demonstrated that the climatic dimension is more important than the species interaction dimension for niche differentiation of these cryptic pathogens. A field heating experiment showed strong seasonal change in the structure of the foliar fungal community, with experimental warming playing an important role in driving this change. This experiment also revealed that warming and plant genotype jointly shape plant phenology, disease levels and insect abundance across the growing season.

In conclusion, my findings suggest that abiotic forces can override biotic forces in structuring spatial patterns and temporal dynamics of fungal communities associated with plants. The particularly strong impact of warmer temperatures on foliar fungi in some of my studies indicates that climate warming has the potential to structure foliar fungal communities, with important implications for plant health, interactions between plants and other organisms and ecosystem functions.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2021. p. 39
Keywords
abiotic and biotic forces, climate warming, community ecology, foliar fungal community, host genotype, plant microbiome, powdery mildew, seasonal dynamics, warming-by-genotype interaction, Quercus robur, soil fungal community, spatial patterns
National Category
Ecology
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-190746 (URN)978-91-7911-412-1 (ISBN)978-91-7911-413-8 (ISBN)
Public defence
2021-04-16, online via zoom, a link will be published a few days before the defence at https://www.su.se/deep/, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2021-03-24 Created: 2021-03-01 Last updated: 2022-02-25Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0001-8206-9332

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