Krista L. McGuire

Digging the New York City Skyline: soil fungal communities in green roofs and city parks.

In urban environments, green roofs provide a number of benefits, including decreased urban heat island effects and reduced energy costs for buildings. However, little research has been done on the non-plant biota associated with green roofs, which likely affect their functionality. For the current study, we evaluated whether or not green roofs planted with two native plant communities in New York City functioned as habitats for soil fungal communities, and compared fungal communities in green roof growing media to soil microbial composition in five city parks, including Central Park and the High Line. Ten replicate roofs were sampled one year after planting; three of these roofs were more intensively sampled and compared to nearby city parks. Using Illumina sequencing of the fungal ITS region we found that green roofs supported a diverse fungal community, with numerous taxa belonging to fungal groups capable of surviving in disturbed and polluted habitats. Across roofs, there was significant biogeographical clustering of fungal communities, indicating that community assembly of roof microbes across the greater New York City area is locally variable. Green roof fungal communities were compositionally distinct from city parks and only 54% of the green roof taxa were also found in the park soils. Phospholipid fatty acid analysis revealed that park soils had greater microbial biomass and higher bacterial to fungal ratios than green roof substrates. City park soils were also more enriched with heavy metals, had lower pH, and lower quantities of total bases (Ca, K, and Mg) compared to green roof substrates. While fungal communities were compositionally distinct across green roofs, they did not differentiate by plant community. Together, these results suggest that fungi living in the growing medium of green roofs may be an underestimated component of these biotic systems functioning to support some of the valued ecological services of green roofs.

Functional diversity in resource use by fungi

Fungi influence nutrient cycling in terrestrial ecosystems, as they are major regulators of decomposition and soil respiration. However, little is known about the substrate preferences of individual fungal species outside of laboratory culture studies. If active fungi differ in their substrate preferences in situ, then changes in fungal diversity due to global change may dramatically influence nutrient cycling in ecosystems. To test the responses of individual fungal taxa to specific substrates, we used a nucleotide-analogue procedure in the boreal forest of Alaska (USA). Specifically, we added four organic N compounds commonly found in plant litter (arginine, glutamate, lignocellulose, and tannin-protein) to litterbags filled with decomposed leaf litter (black spruce and aspen) and assessed the responses of active fungal species using qPCR (quantitative polymerase chain reaction), oligonucleotide fingerprinting of rRNA genes, and sequencing. We also compared the sequences from our experiment with a concurrent warming experiment to see if active fungi that targeted more recalcitrant compounds would respond more positively to soil warming. We found that individual fungal taxa responded differently to substrate additions and that active fungal communities were different across litter types (spruce vs. aspen). Active fungi that targeted lignocellulose also responded positively to experimental warming. Additionally, resource-use patterns in different fungal taxa were genetically correlated, suggesting that it may be possible to predict the ecological function of active fungal communities based on genetic information. Together, these results imply that fungi are functionally diverse and that reductions in fungal diversity may have consequences for ecosystem functioning.

Relating belowground microbial composition to the taxonomic, phylogenetic, and functional trait distributions of trees in a tropical forest

The complexities of the relationships between plant and soil microbial communities remain unresolved. We determined the associations between plant aboveground and belowground (root) distributions and the communities of soil fungi and bacteria found across a diverse tropical forest plot. Soil microbial community composition was correlated with the taxonomic and phylogenetic structure of the aboveground plant assemblages even after controlling for differences in soil characteristics, but these relationships were stronger for fungi than for bacteria. In contrast to expectations, the species composition of roots in our soil core samples was a poor predictor of microbial community composition perhaps due to the patchy, ephemeral, and highly overlapping nature of fine root distributions. Our ability to predict soil microbial composition was not improved by incorporating information on plant functional traits suggesting that the most commonly measured plant traits are not particularly useful for predicting the plot-level variability in belowground microbial communities.

Effects of industrial agriculture on climate change and the mitigation potential of small-scale agro-ecological farms

According to the Intergovernmental Panel on Climate Change (IPCC), agriculture is responsible for 10–12% of total global anthropogenic emissions and almost a quarter of the continuing increase of greenhouse gas (GHG) emissions. Not all forms of agriculture, however, have equivalent impacts on global warming. Industrial agriculture contributes significantly to global warming, representing a large majority of total agriculture-related GHG emissions. Alternatively, ecologically based methods for agricultural production, predominantly used on small-scale farms, are far less energy-consumptive and release fewer GHGs than industrial agricultural production. Besides generating fewer direct emissions, agro-ecological management techniques have the potential to sequester more GHGs than industrial agriculture. Here, we review the literature on the contributions of agriculture to climate change and show the extent of GHG contributions from the industrial agricultural system and the potential of agro-ecological smallholder agriculture to help reduce GHG emissions. These reductions are achieved in three broad areas when compared with the industrial agricultural system: (1) a decrease in materials used and fluxes involved in the release of GHGs based on agricultural crop management choices; (2) a decrease in fluxes involved in livestock production and pasture management; and (3) a reduction in the transportation of agricultural inputs, outputs and products through an increased emphasis on local food systems. Although there are a number of barriers and challenges towards adopting small-scale agroecological methods on the large scale, appropriate incentives can lead to incremental steps towards agro-ecological management that may be able to reduce and mitigate GHG emissions from the agricultural sector.

Ectomycorrhizal-Dominated Boreal and Tropical Forests Have Distinct Fungal Communities, but Analogous Spatial Patterns across Soil Horizons

Fungi regulate key nutrient cycling processes in many forest ecosystems, but their diversity and distribution within and across ecosystems are poorly understood. Here, we examine the spatial distribution of fungi across a boreal and tropical ecosystem, focusing on ectomycorrhizal fungi. We analyzed fungal community composition across litter (organic horizons) and underlying soil horizons (0–20 cm) using 454 pyrosequencing and clone library sequencing. In both forests, we found significant clustering of fungal communities by site and soil horizons with analogous patterns detected by both sequencing technologies. Free-living saprotrophic fungi dominated the recently-shed leaf litter and ectomycorrhizal fungi dominated the underlying soil horizons. This vertical pattern of fungal segregation has also been found in temperate and European boreal forests, suggesting that these results apply broadly to ectomycorrhizal-dominated systems, including tropical rain forests. Since ectomycorrhizal and free-living saprotrophic fungi have different influences on soil carbon and nitrogen dynamics, information on the spatial distribution of these functional groups will improve our understanding of forest nutrient cycling.

Evolutionary histories of soil fungi are reflected in their large- scale biogeography

Although fungal communities are known to vary along latitudinal gradients, mechanisms underlying this pattern are not well-understood. We used high-throughput sequencing to examine the large-scale distributions of soil fungi and their relation to evolutionary history. We tested the Tropical Conservatism Hypothesis, which predicts that ancestral fungal groups should be more restricted to tropical latitudes and conditions than would more recently derived groups. We found support for this hypothesis in that older phyla preferred significantly lower latitudes and warmer, wetter conditions than did younger phyla. Moreover, preferences for higher latitudes and lower precipitation levels were significantly phylogenetically conserved among the six younger phyla, possibly because the older phyla possess a zoospore stage that is vulnerable to drought, whereas the younger phyla retain protective cell walls throughout their life cycle. Our study provides novel evidence that the Tropical Conservatism Hypothesis applies to microbes as well as plants and animals.

Agricultural intensification and the functional capacity of soil microbes on smallholder African farms

Summary 1. Fertilization may impact ecosystem processes that sustain agriculture, such as nutrient cycling, by altering the composition of soil microbial communities that regulate such processes. These processes are crucial to low-input, smallholder tropical agriculture, which supports 900 million of the world’s poorest people. Yet little is known about how efforts to increase crop yield on such farms will affect the capacity of soil microbial communities to carry out ecosystem processes. 2. We studied the diversity and functional capacity of microbial communities on smallholder farms in western Kenya. We measured functional capacity as the abundance of functional genes involved in several components of nutrient cycling as well as catabolism of multiple carbon substrates; taxonomic diversity was measured using metagenomic sequencing. Diversity and functional capacity were measured on short-term, experimental mineral fertilizer addition plots and on actively managed farms that have maintained for at least seven years a management strategy of low mineral fertilization, high mineral fertilization, or high fertilization combined with legume rotations. 3. Soil bacterial diversity decreased with mineral fertilizer addition, with a community shift towards taxa that thrive in high-resource conditions. This taxonomic response did not correspond with decreased microbial functional capacity. Instead, functional capacity was increased, along with yields, when fertilizers were combined with legume rotations that add organic matter to soil. 4. Policy implications. Mineral fertilizer use is associated with lower soil microbial diversity on smallholder farms, but not associated with changes in microbial functional capacity. Functional capacity is highest, along with yields, when mineral fertilizers are paired with legume rotations. Our findings suggest that this type of agroforestry can be an important strategy for maintaining the long-term functional capacity of soil microbes as well as increasing crop yields on smallholder farms. These observations support proposals to achieve long-term food production targets in sub-Saharan Africa by combining mineral fertilizers with organic inputs.

Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity

Significance Bacterial natural products (NPs) have served as inspiration for many therapeutics. The hunt for new bioactive NPs has led to a global search for natural ecosystems from which bacteria can be cultured. Here, we used NP-focused metagenome sequencing to explore biosynthetic diversity in urban park soil of New York City. Our analyses reveal rich biosynthetic diversity in these microbiomes and predict that gene clusters encoding many clinically approved NPs families discovered using bacteria cultured from around the world are actually present in the soil microbiomes of a single city. Contrary to traditional NP discovery efforts that involve shallow explorations of diverse environments, our data suggest that a deeper exploration of local microbiomes may prove equally, if not, more productive. Numerous therapeutically relevant small molecules have been identified from the screening of natural products (NPs) produced by environmental bacteria. These discovery efforts have principally focused on culturing bacteria from natural environments rich in biodiversity. We sought to assess the biosynthetic capacity of urban soil environments using a phylogenetic analysis of conserved NP biosynthetic genes amplified directly from DNA isolated from New York City park soils. By sequencing genes involved in the biosynthesis of nonribosomal peptides and polyketides, we found that urban park soil microbiomes are both rich in biosynthetic diversity and distinct from nonurban samples in their biosynthetic gene composition. A comparison of sequences derived from New York City parks to genes involved in the biosynthesis of biomedically important NPs produced by bacteria originally collected from natural environments around the world suggests that bacteria producing these same families of clinically important antibiotics, antifungals, and anticancer agents are actually present in the soils of New York City. The identification of new bacterial NPs often centers on the systematic exploration of bacteria present in natural environments. Here, we find that the soil microbiomes found in large cities likely hold similar promise as rich unexplored sources of clinically relevant NPs.

Farm management, not soil microbial diversity, controls nutrient loss from smallholder tropical agriculture

Tropical smallholder agriculture is undergoing rapid transformation in nutrient cycling pathways as international development efforts strongly promote greater use of mineral fertilizers to increase crop yields. These changes in nutrient availability may alter the composition of microbial communities with consequences for rates of biogeochemical processes that control nutrient losses to the environment. Ecological theory suggests that altered microbial diversity will strongly influence processes performed by relatively few microbial taxa, such as denitrification and hence nitrogen losses as nitrous oxide, a powerful greenhouse gas. Whether this theory helps predict nutrient losses from agriculture depends on the relative effects of microbial community change and increased nutrient availability on ecosystem processes. We find that mineral and organic nutrient addition to smallholder farms in Kenya alters the taxonomic and functional diversity of soil microbes. However, we find that the direct effects of farm management on both denitrification and carbon mineralization are greater than indirect effects through changes in the taxonomic and functional diversity of microbial communities. Changes in functional diversity are strongly coupled to changes in specific functional genes involved in denitrification, suggesting that it is the expression, rather than abundance, of key functional genes that can serve as an indicator of ecosystem process rates. Our results thus suggest that widely used broad summary statistics of microbial diversity based on DNA may be inappropriate for linking microbial communities to ecosystem processes in certain applied settings. Our results also raise doubts about the relative control of microbial composition compared to direct effects of management on nutrient losses in applied settings such as tropical agriculture.

Responses of sugar maple and hemlock seedlings to elevated carbon dioxide under altered above- and belowground nitrogen sources

Various human-induced changes to the atmosphere have caused carbon dioxide (CO₂), nitrogen dioxide (NO₂) and nitrate deposition (NO₃⁻) to increase in many regions of the world. The goal of this study was to examine the simultaneous influence of these three factors on tree seedlings. We used open-top chambers to fumigate sugar maple (Acer saccharum) and eastern hemlock (Tsuga canadensis) with ambient or elevated CO₂ and NO₂ (elevated concentrations were 760 ppm and 40 ppb, respectively). In addition, we applied an artificial wet deposition of 30 kg ha⁻¹ year⁻¹ NO₃⁻ to half of the open-top chambers. After two growing seasons, hemlocks showed a stimulation of growth under elevated CO₂, but the addition of elevated NO₂ or NO₃⁻ eliminated this effect. In contrast, sugar maple seedlings showed no growth enhancement under elevated CO₂ alone and decreased growth in the presence of NO₂ or NO₃⁻, and the combined treatments of elevated CO₂ with increased NO₂ or NO₃⁻ were similar to control plants. Elevated CO₂ induced changes in the leaf characteristics of both species, including decreased specific leaf area, decreased %N and increased C:N. The effects of elevated CO₂, NO₂ and NO₃⁻ on growth were not additive and treatments that singly had no effect often modified the effects of other treatments. The growth of both maple and hemlock seedlings under the full combination of treatments (CO₂ + NO₂ + NO₃⁻) was similar to that of seedlings grown under control conditions, suggesting that models predicting increased seedling growth under future atmospheric conditions may be overestimating the growth and carbon storage potential of young trees.