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  1. Free, publicly-accessible full text available September 1, 2024
  2. 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.

     
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    Free, publicly-accessible full text available September 5, 2024
  3. Free, publicly-accessible full text available April 1, 2024
  4. Projections for the northeastern United States indicate that mean air temperatures will rise and snowfall will become less frequent, causing more frequent soil freezing. To test fungal responses to these combined chronic and extreme soil temperature changes, we conducted a laboratory-based common garden experiment with soil fungi that had been subjected to different combinations of growing season soil warming, winter soil freeze/thaw cycles, and ambient conditions for 4 years in the field. We found that fungi originating from field plots experiencing a combination of growing season warming and winter freeze/thaw cycles had inherently lower activity of acid phosphatase, but higher cellulase activity, that could not be reversed in the lab. In addition, fungi quickly adjusted their physiology to freeze/thaw cycles in the laboratory, reducing growth rate, and potentially reducing their carbon use efficiency. Our findings suggest that less than 4 years of new soil temperature conditions in the field can lead to physiological shifts by some soil fungi, as well as irreversible loss or acquisition of extracellular enzyme activity traits by other fungi. These findings could explain field observations of shifting soil carbon and nutrient cycling under simulated climate change. 
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  5. Projections for the northeastern U.S. indicate that mean air temperatures will rise and snowfall will become less frequent, causing more frequent soil freezing. To test fungal responses to these combined chronic and extreme soil temperature changes, we conducted a laboratory-based common garden experiment with soil fungi that had been subjected to different combinations of growing season soil warming, winter soil freeze/thaw cycles, and ambient conditions for four years in the field. We found that fungi originating from field plots experiencing a combination of growing season warming and winter freeze/thaw cycles had inherently lower activity of acid phosphatase, but higher cellulase activity, that could not be reversed in the lab. In addition, fungi quickly adjusted their physiology to freeze/thaw cycles in the laboratory, reducing growth rate and potentially reducing their carbon use efficiency. Our findings suggest that less than four years of new soil temperature conditions in the field can lead to physiological shifts by some soil fungi, as well as irreversible loss or acquisition of extracellular enzyme activity traits by other fungi. These findings could explain field observations of shifting soil carbon and nutrient cycling under simulated climate change. These data were gathered as part of the Hubbard Brook Ecosystem Study (HBES). The HBES is a collaborative effort at the Hubbard Brook Experimental Forest, which is operated and maintained by the USDA Forest Service, Northern Research Station. 
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  6. Summary

    Iron (Fe) is crucial for metabolic functions of living organisms. Plants access occluded Fe through interactions with rhizosphere microorganisms and symbionts. Yet, the interplay between Fe addition and plant–mycorrhizal interactions, especially the molecular mechanisms underlying mycorrhiza‐assisted Fe processing in plants, remains largely unexplored.

    We conducted mesocosms inPinusplants inoculated with different ectomycorrhizal fungi (EMF)Suillusspecies under conditions with and without Fe coatings. Meta‐transcriptomic, biogeochemical, and X‐ray fluorescence imaging analyses were applied to investigate early‐stage mycorrhizal roots.

    While Fe addition promotedPinusgrowth, it concurrently reduced mycorrhiza formation rate, symbiosis‐related metabolites in plant roots, and aboveground plant carbon and macronutrient content. This suggested potential trade‐offs between Fe‐enhanced plant growth and symbiotic performance. However, the extent of this trade‐off may depend on interactions between host plants and EMF species. Interestingly, dual EMF species were more effective at facilitating plant Fe uptake by inducing diverse Fe‐related functions than single‐EMF species. This subsequently triggered various Fe‐dependent physiological and biochemical processes inPinusroots, significantly contributing toPinusgrowth. However, this resulted in a greater carbon allocation to roots, relatively reducing the aboveground plant carbon content.

    Our study offers critical insights into how EMF communities rebalance benefits of Fe‐induced effects on symbiotic partners.

     
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  7. Metagenomes encode an enormous diversity of proteins, reflecting a multiplicity of functions and activities. Exploration of this vast sequence space has been limited to a comparative analysis against reference microbial genomes and protein families derived from those genomes. Here, to examine the scale of yet untapped functional diversity beyond what is currently possible through the lens of reference genomes, we develop a computational approach to generate reference-free protein families from the sequence space in metagenomes. We analyze 26,931 metagenomes and identify 1.17 billion protein sequences longer than 35 amino acids with no similarity to any sequences from 102,491 reference genomes or the Pfam database. Using massively parallel graph-based clustering, we group these proteins into 106,198 novel sequence clusters with more than 100 members, doubling the number of protein families obtained from the reference genomes clustered using the same approach. We annotate these families on the basis of their taxonomic, habitat, geographical, and gene neighborhood distributions and, where sufficient sequence diversity is available, predict protein three-dimensional models, revealing novel structures. Overall, our results uncover an enormously diverse functional space, highlighting the importance of further exploring the microbial functional dark matter. 
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    Free, publicly-accessible full text available October 19, 2024