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      Soil Metatranscriptomes Under Long-Term Experimental Warming and Drying: Fungi Allocate Resources to Cell Metabolic Maintenance Rather Than Decay

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          Abstract

          Earth’s temperature is rising, and with this increase, fungal communities are responding and affecting soil carbon processes. At a long-term soil-warming experiment in a boreal forest in interior Alaska, warming and warming-associated drying alters the function of microbes, and thus, decomposition of carbon. But what genetic mechanisms and resource allocation strategies are behind these community shifts and soil carbon changes? Here, we evaluate fungal resource allocation efforts under long-term experimental warming (including associated drying) using soil metatranscriptomics. We profiled resource allocation efforts toward decomposition and cell metabolic maintenance, and we characterized community composition. We found that under the warming treatment, fungi allocate resources to cell metabolic maintenance at the expense of allocating resources to decomposition. In addition, we found that fungal orders that house taxa with stress-tolerant traits were more abundant under the warmed treatment compared to control conditions. Our results suggest that the warming treatment elicits an ecological tradeoff in resource allocation in the fungal communities, with potential to change ecosystem-scale carbon dynamics. Fungi preferentially invest in mechanisms that will ensure survival under warming and drying, such as cell metabolic maintenance, rather than in decomposition. Through metatranscriptomes, we provide mechanistic insight behind the response of fungi to climate change and consequences to soil carbon processes.

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          Most cited references 67

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          IMG/M: integrated genome and metagenome comparative data analysis system

          The Integrated Microbial Genomes with Microbiome Samples (IMG/M: https://img.jgi.doe.gov/m/) system contains annotated DNA and RNA sequence data of (i) archaeal, bacterial, eukaryotic and viral genomes from cultured organisms, (ii) single cell genomes (SCG) and genomes from metagenomes (GFM) from uncultured archaea, bacteria and viruses and (iii) metagenomes from environmental, host associated and engineered microbiome samples. Sequence data are generated by DOE's Joint Genome Institute (JGI), submitted by individual scientists, or collected from public sequence data archives. Structural and functional annotation is carried out by JGI's genome and metagenome annotation pipelines. A variety of analytical and visualization tools provide support for examining and comparing IMG/M's datasets. IMG/M allows open access interactive analysis of publicly available datasets, while manual curation, submission and access to private datasets and computationally intensive workspace-based analysis require login/password access to its expert review (ER) companion system (IMG/M ER: https://img.jgi.doe.gov/mer/). Since the last report published in the 2014 NAR Database Issue, IMG/M's dataset content has tripled in terms of number of datasets and overall protein coding genes, while its analysis tools have been extended to cope with the rapid growth in the number and size of datasets handled by the system.
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            Active and total microbial communities in forest soil are largely different and highly stratified during decomposition.

            Soils of coniferous forest ecosystems are important for the global carbon cycle, and the identification of active microbial decomposers is essential for understanding organic matter transformation in these ecosystems. By the independent analysis of DNA and RNA, whole communities of bacteria and fungi and its active members were compared in topsoil of a Picea abies forest during a period of organic matter decomposition. Fungi quantitatively dominate the microbial community in the litter horizon, while the organic horizon shows comparable amount of fungal and bacterial biomasses. Active microbial populations obtained by RNA analysis exhibit similar diversity as DNA-derived populations, but significantly differ in the composition of microbial taxa. Several highly active taxa, especially fungal ones, show low abundance or even absence in the DNA pool. Bacteria and especially fungi are often distinctly associated with a particular soil horizon. Fungal communities are less even than bacterial ones and show higher relative abundances of dominant species. While dominant bacterial species are distributed across the studied ecosystem, distribution of dominant fungi is often spatially restricted as they are only recovered at some locations. The sequences of cbhI gene encoding for cellobiohydrolase (exocellulase), an essential enzyme for cellulose decomposition, were compared in soil metagenome and metatranscriptome and assigned to their producers. Litter horizon exhibits higher diversity and higher proportion of expressed sequences than organic horizon. Cellulose decomposition is mediated by highly diverse fungal populations largely distinct between soil horizons. The results indicate that low-abundance species make an important contribution to decomposition processes in soils.
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              The genome portal of the Department of Energy Joint Genome Institute: 2014 updates

              The U.S. Department of Energy (DOE) Joint Genome Institute (JGI), a national user facility, serves the diverse scientific community by providing integrated high-throughput sequencing and computational analysis to enable system-based scientific approaches in support of DOE missions related to clean energy generation and environmental characterization. The JGI Genome Portal (http://genome.jgi.doe.gov) provides unified access to all JGI genomic databases and analytical tools. The JGI maintains extensive data management systems and specialized analytical capabilities to manage and interpret complex genomic data. A user can search, download and explore multiple data sets available for all DOE JGI sequencing projects including their status, assemblies and annotations of sequenced genomes. Here we describe major updates of the Genome Portal in the past 2 years with a specific emphasis on efficient handling of the rapidly growing amount of diverse genomic data accumulated in JGI.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                20 August 2019
                2019
                : 10
                Affiliations
                1Department of Ecology and Evolutionary Biology, University of California, Irvine , Irvine, CA, United States
                2Department of Electronics and Telecommunications, Ensenada Center for Scientific Research and Higher Education , Ensenada, Mexico
                3Department of Medical Innovation, Ensenada Center for Scientific Research and Higher Education , Ensenada, Mexico
                Author notes

                Edited by: Martin Hartmann, ETH Zurich, Switzerland

                Reviewed by: Petr Baldrian, Institute of Microbiology of the ASCR, Czechia; Ivano Brunner, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Switzerland

                *Correspondence: Adriana L. Romero-Olivares, Adriana.RomeroOlivares@ 123456unh.edu ; adrilu.romero@ 123456gmail.com

                This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.01914
                6736569
                Copyright © 2019 Romero-Olivares, Meléndrez-Carballo, Lago-Lestón and Treseder.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 85, Pages: 9, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology

                cog, tradeoff, fungi, soil carbon, decomposition, global warming, cazy, metatranscriptome

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