Microbial carbon use efficiency predicted from genome-scale metabolic models

Respiration by soil bacteria and fungi is one of the largest fluxes of carbon (C) from the land surface. Although this flux is a direct product of microbial metabolism, controls over metabolism and their responses to global change are a major uncertainty in the global C cycle. Here, we explore an in silico approach to predict bacterial C-use efficiency (CUE) for over 200 species using genome-specific constraint-based metabolic modeling. We find that potential CUE averages 0.62 ± 0.17 with a range of 0.22 to 0.98 across taxa and phylogenetic structuring at the subphylum levels. Potential CUE is negatively correlated with genome size, while taxa with larger genomes are able to access a wider variety of C substrates. Incorporating the range of CUE values reported here into a next-generation model of soil biogeochemistry suggests that these differences in physiology across microbial taxa can feed back on soil-C cycling.Published versio

Composition of fungal functional guilds explains variance in forest soil nutrient cycling

Soil fungi and bacteria are responsible for soil nutrient cycling, including decomposition, mineralization, immobilization, and transfer of nutrients to tree roots, yet the role of soil community composition in controlling forest nutrient cycling is poorly understood. We aimed to test the hypothesis that incorporating microbial community composition into linear models will increase the variation explained in forest soil N and P cycling relative to models including only plant community and abiotic characteristics. To do this, we designed a forested field system in New England in which variation in microbial community composition was crossed with variation in vegetation composition and soil nutrient content. At six forest sites (three suburban and three rural sites), we sampled soil along a transect from the forest edge to interior from four stand types dominated by trees of varying litter quality: pine-dominated, pure hardwood, hardwood with pines in the understory, and mature mixed pine-hardwood. In each soil sample, we measured inorganic and total nitrogen (N) and phosphorus (P), N and P mineralization rates, and nitrification rates. We also performed high-throughput sequencing of fungal and bacterial rDNA amplicons (16S/ITS) and calculated functional guild abundance for fungi and bacteria in each sample. Excluding microbial factors, N mineralization was best explained in a linear model by pH, soil temperature, soil moisture, % soil organic matter, and the abundance of understory vegetation; nitrification was best explained by pH, the proportion of hardwood litter, the abundance of understory vegetation, and basal area of arbuscular mycorrhizal-associating trees. We found that including the proportion of fungal functional guilds improved linear statistical models explaining variance in rates of N mineralization and nitrification, but not in single point measurements of inorganic N or total P. The proportion of ectomycorrhizal fungi per sample was positively related to N mineralization (p = 7e-05, R2 = 0.128), and including it in the model increased the proportion of variance explained in N mineralization rates by 2.8%. The proportion of saprotrophic fungi per sample was positively related to nitrification (p = 0.001, R2 = 0.083), and including it in the model increased the proportion of variance explained in nitrification rates by 2.0%. These findings suggest that ectomycorrhizal fungi may play a role in N mineralization, while saprotrophs may be more important for nitrification. We are currently building models to explain P mineralization and to improve current models by incorporating bacterial functional guilds.Fil: Vietorisz, Corinne. Boston University; Estados UnidosFil: Policelli, Nahuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; Argentina. Boston University; Estados UnidosFil: Li, Abigail. Boston University; Estados UnidosFil: Adams, Lindsey. Boston University; Estados UnidosFil: Bhatnagar, Jennifer M.. Boston University; Estados UnidosESA 2023 - Meeting of the Ecological Society of AmericaPortlandEstados UnidosEcological Society of Americ

Multi-omic Analyses of Extensively Decayed Pinus contorta Reveal Expression of a Diverse Array of Lignocellulose-Degrading Enzymes.

Fungi play a key role cycling nutrients in forest ecosystems, but the mechanisms remain uncertain. To clarify the enzymatic processes involved in wood decomposition, the metatranscriptomics and metaproteomics of extensively decayed lodgepole pine were examined by RNA sequencing (RNA-seq) and liquid chromatography-tandem mass spectrometry (LC-MS/MS), respectively. Following de novo metatranscriptome assembly, 52,011 contigs were searched for functional domains and homology to database entries. Contigs similar to basidiomycete transcripts dominated, and many of these were most closely related to ligninolytic white rot fungi or cellulolytic brown rot fungi. A diverse array of carbohydrate-active enzymes (CAZymes) representing a total of 132 families or subfamilies were identified. Among these were 672 glycoside hydrolases, including highly expressed cellulases or hemicellulases. The CAZymes also included 162 predicted redox enzymes classified within auxiliary activity (AA) families. Eighteen of these were manganese peroxidases, which are key components of ligninolytic white rot fungi. The expression of other redox enzymes supported the working of hydroquinone reduction cycles capable of generating reactive hydroxyl radicals. These have been implicated as diffusible oxidants responsible for cellulose depolymerization by brown rot fungi. Thus, enzyme diversity and the coexistence of brown and white rot fungi suggest complex interactions of fungal species and degradative strategies during the decay of lodgepole pine.IMPORTANCE The deconstruction of recalcitrant woody substrates is a central component of carbon cycling and forest health. Laboratory investigations have contributed substantially toward understanding the mechanisms employed by model wood decay fungi, but few studies have examined the physiological processes in natural environments. Herein, we identify the functional genes present in field samples of extensively decayed lodgepole pine (Pinus contorta), a major species distributed throughout the North American Rocky Mountains. The classified transcripts and proteins revealed a diverse array of oxidative and hydrolytic enzymes involved in the degradation of lignocellulose. The evidence also strongly supports simultaneous attack by fungal species employing different enzymatic strategies

Does elevated CO2 alter the way microbes behave underground?

Increase in carbon (C) emissions due to human activity is a major cause of global change, but it is unclear how trees obtain soil nutrients to sustain growth under these conditions. To better understand how root symbiotic fungi (ectomycorrhizal fungi, EMF) will react to an increase in atmospheric CO2 we’ve simulated such scenario using synthetic ecosystems where pine trees were planted with and without their EMF (Suillus cothurnatus), nitrogen (N), and soil carbon (C) additions, in elevated vs ambient CO2 growth chambers. By combining biogeochemical analysis with differential isotopic signatures of soil vs plant C, and a series of -omic approaches, we captured changes in soil nutrients, soil respiration, and microbial composition and activity. We found that elevated CO2 did not lead to a change in free living fungal community composition compared to ambient CO2. However, under elevated CO2, more gene modules of S. cothurnatus involved in C-N degradation pathways were impacted by soil C and N additions. In turn, under elevated CO2 and when the EMF was present, we found high enrichment of non-targeted metabolites. The release of CO2 from soil was highly dependent on soil C and N availability and shifted depending on plant C availability. Our results inform ecosystem models by showing that interactions between free living fungi and EMF are an important mechanism for determining ecosystem responses to elevated CO2. In turn, our results challenge the classic perspective that EMF solely absorb nutrients and water and give them to plants.Fil: Policelli, Nahuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; Argentina. Boston University; Estados UnidosFil: Averill, Colin. Eidgenossische Technische Hochschule zurich (eth Zurich);Fil: Brzostek, Edward. West Virginia University; Estados UnidosFil: Wang, Haihua. University of Florida; Estados UnidosFil: Liao, Hui-Ling. University of Florida; Estados UnidosFil: Verma, Vijay. University of Florida; Estados UnidosFil: Tappero, Ryan. Brookhaven National Laboratory; Estados UnidosFil: Vietorisz, Corinne. Boston University; Estados UnidosFil: Nash, Jake. University of Duke; Estados UnidosFil: Vilgalys, Rytas. University of Duke; Estados UnidosFil: Bhatnagar, Jennifer M.. Boston University; Estados UnidosESA 2023 - Meeting of the Ecological Society of AmericaPortlandEstados UnidosEcological Society of Americ

Back to Roots: The Role of Ectomycorrhizal Fungi in Boreal and Temperate Forest Restoration

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Global Imprint of Mycorrhizal Fungi on Whole-Plant Nutrient Economics

Mycorrhizal fungi are critical members of the plant microbiome, forming a symbiosis with the roots of most plants on Earth. Most plant species partner with either arbuscular or ectomycorrhizal fungi, and these symbioses are thought to represent plant adaptations to fast and slow soil nutrient cycling rates. This generates a second hypothesis, that arbuscular and ectomycorrhizal plant species traits complement and reinforce these fungal strategies, resulting in nutrient acquisitive vs. conservative plant trait profiles. Here we analyzed 17,764 species level trait observations from 2,940 woody plant species to show that mycorrhizal plants differ systematically in nitrogen and phosphorus economic traits. Differences were clearest in temperate latitudes, where ectomycorrhizal plant species are more nitrogen use- and phosphorus use-conservative than arbuscular mycorrhizal species. This difference is reflected in both aboveground and belowground plant traits and is robust to controlling for evolutionary history, nitrogen fixation ability, deciduousness, latitude, and species climate niche. Furthermore, mycorrhizal effects are large and frequently similar to or greater in magnitude than the influence of plant nitrogen fixation ability or deciduous vs. evergreen leaf habit. Ectomycorrhizal plants are also more nitrogen conservative than arbuscular plants in boreal and tropical ecosystems, although differences in phosphorus use are less apparent outside temperate latitudes. Our findings bolster current theories of ecosystems rooted in mycorrhizal ecology and support the hypothesis that plant mycorrhizal association is linked to the evolution of plant nutrient economic strategies

Ectomycorrhizal Plant-Fungal Co-invasions as Natural Experiments for Connecting Plant and Fungal Traits to Their Ecosystem Consequences

Introductions and invasions by fungi, especially pathogens and mycorrhizal fungi, are widespread and potentially highly consequential for native ecosystems, but may also offer opportunities for linking microbial traits to their ecosystem functions. In particular, treating ectomycorrhizal (EM) invasions, i.e., co-invasions by EM fungi and their EM host plants, as natural experiments may offer a powerful approach for testing how microbial traits influence ecosystem functions. Forests dominated by EM symbiosis have unique biogeochemistry whereby the secretions of EM plants and fungi affect carbon (C) and nutrient cycling; moreover, particular lineages of EM fungi have unique functional traits. EM invasions may therefore alter the biogeochemistry of the native ecosystems they invade, especially nitrogen (N) and C cycling. By identifying “response traits” that favor the success of fungi in introductions and invasions (e.g., spore dispersal and germination) and their correlations with “effect traits” (e.g., nutrient-cycling enzymes) that can alter N and C cycling (and affect other coupled elemental cycles), one may be able to predict the functional consequences for ecosystems of fungal invasions using biogeochemistry models that incorporate fungal traits. Here, we review what is already known about how EM fungal community composition, traits, and ecosystem functions differ between native and exotic populations, focusing on the example of EM fungi associated with species of Pinus introduced from the Northern into the Southern Hemisphere. We develop hypotheses on how effects of introduced and invasive EM fungi may depend on interactions between soil N availability in the exotic range and EM fungal traits. We discuss how such hypotheses could be tested by utilizing Pinus introductions and invasions as a model system, especially when combined with controlled laboratory experiments. Finally, we illustrate how ecosystem modeling can be used to link fungal traits to their consequences for ecosystem N and C cycling in the context of biological invasions, and we highlight exciting avenues for future directions in understanding EM invasion.Fil: Hoeksema, Jason D.. University of Mississippi; Estados UnidosFil: Averill, Colin. No especifíca;Fil: Bhatnagar, Jennifer M.. Boston University; Estados UnidosFil: Brzostek, Edward. West Virginia University; Estados UnidosFil: Buscardo, Erika. Universidade do Brasília; BrasilFil: Chen, Ko Hsuan. University of Florida; Estados UnidosFil: Liao, Hui Ling. University of Florida; Estados UnidosFil: Nagy, Laszlo. Universidade Estadual de Campinas; BrasilFil: Policelli, Nahuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Ridgeway, Joanna. West Virginia University; Estados UnidosFil: Rojas, J. Alejandro. University of Arkansas for Medical Sciences; Estados UnidosFil: Vilgalys, Rytas. University of Duke; Estados Unido

Fecal Microbial Communities in a Large Representative Cohort of California Dairy Cows

Improved sequencing and analytical techniques allow for better resolution of microbial communities; however, the agriculture field lacks an updated analysis surveying the fecal microbial populations of dairy cattle in California. This study is a large-scale survey to determine the composition of the bacterial community present in the feces of lactating dairy cattle on commercial dairy operations. For the study, 10 dairy farms across northern and central California representing a variety of feeding and management systems were enrolled. The farms represented three typical housing types including five freestall, two drylot and three pasture-based management systems. Fresh feces were collected from 15 randomly selected cows on each farm and analyzed using 16S rRNA gene amplicon sequencing. This study found that housing type, individual farm, and dietary components significantly affected the alpha diversity of the fecal microbiota. While only one Operational Taxonomic Unit (OTU) was common among all the sampled individuals, 15 bacterial families and 27 genera were shared among 95% of samples. The ratio of the families Coriobacteriaceae to Bifidobacteriaceae was significantly different between housing types and farms with pasture fed animals having a higher relative abundance of Coriobacteriaceae. A majority of samples were positive for at least one OTU assigned to Enterobacteriaceae and 31% of samples contained OTUs assigned to Campylobacter. However, the relative abundance of both taxa was <0.1%. The microbial composition displays individual farm specific signatures, but housing type plays a role. These data provide insights into the composition of the core fecal microbiota of commercial dairy cows in California and will further generate hypotheses for strategies to manipulate the microbiome of cattle

Roots Mediate the Effects of Snowpack Decline on Soil Bacteria, Fungi, and Nitrogen Cycling in a Northern Hardwood Forest

Rising winter air temperature will reduce snow depth and duration over the next century in northern hardwood forests. Reductions in snow depth may affect soil bacteria and fungi directly, but also affect soil microbes indirectly through effects of snowpack loss on plant roots. We incubated root exclusion and root ingrowth cores across a winter climate-elevation gradient in a northern hardwood forest for 29 months to identify direct (i.e., winter snow-mediated) and indirect (i.e., root-mediated) effects of winter snowpack decline on soil bacterial and fungal communities, as well as on potential nitrification and net N mineralization rates. Both winter snowpack decline and root exclusion increased bacterial richness and phylogenetic diversity. Variation in bacterial community composition was best explained by differences in winter snow depth or soil frost across elevation. Root ingrowth had a positive effect on the relative abundance of several bacterial taxonomic orders (e.g., Acidobacterales and Actinomycetales). Nominally saprotrophic (e.g., Saccharomycetales and Mucorales) or mycorrhizal (e.g., Helotiales, Russalales, Thelephorales) fungal taxonomic orders were also affected by both root ingrowth and snow depth variation. However, when grouped together, the relative abundance of saprotrophic fungi, arbuscular mycorrhizal fungi, and ectomycorrhizal fungi were not affected by root ingrowth or snow depth, suggesting that traits in addition to trophic mode will mediate fungal community responses to snowpack decline in northern hardwood forests. Potential soil nitrification rates were positively related to ammonia-oxidizing bacteria and archaea abundance (e.g., Nitrospirales, Nitrosomondales, Nitrosphaerales). Rates of N mineralization were positively and negatively correlated with ectomycorrhizal and saprotrophic fungi, respectively, and these relationships were mediated by root exclusion. The results from this study suggest that a declining winter snowpack and its effect on plant roots each have direct effects on the diversity and abundance of soil bacteria and fungal communities that interact to determine rates of soil N cycling in northern hardwood forests

The global oscillation network group site survey. II. Results

The Global Oscillation Network Group (GONG) Project will place a network of instruments around the world to observe solar oscillations as continuously as possible for three years. The Project has now chosen the six network sites based on analysis of survey data from fifteen sites around the world. The chosen sites are: Big Bear Solar Observatory, California; Mauna Loa Solar Observatory, Hawaii; Learmonth Solar Observatory, Australia; Udaipur Solar Observatory, India; Observatorio del Teide, Tenerife; and Cerro Tololo Interamerican Observatory, Chile. Total solar intensity at each site yields information on local cloud cover, extinction coefficient, and transparency fluctuations. In addition, the performance of 192 reasonable components analysis. An accompanying paper describes the analysis methods in detail; here we present the results of both the network and individual site analyses. The selected network has a duty cycle of 93.3%, in good agreement with numerical simulations. The power spectrum of the network observing window shows a first diurnal sidelobe height of 3 × 10⁻⁴ with respect to the central component, an improvement of a factor of 1300 over a single site. The background level of the network spectrum is lower by a factor of 50 compared to a single-site spectrum