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      Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil

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          Abstract

          Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However, challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and clade-specific patterns of carbon metabolism.

          ABSTRACT

          Soil ecosystems harbor diverse microorganisms and yet remain only partially characterized as neither single-cell sequencing nor whole-community sequencing offers a complete picture of these complex communities. Thus, the genetic and metabolic potential of this “uncultivated majority” remains underexplored. To address these challenges, we applied a pooled-cell-sorting-based mini-metagenomics approach and compared the results to bulk metagenomics. Informatic binning of these data produced 200 mini-metagenome assembled genomes (sorted-MAGs) and 29 bulk metagenome assembled genomes (MAGs). The sorted and bulk MAGs increased the known phylogenetic diversity of soil taxa by 7.2% with respect to the Joint Genome Institute IMG/M database and showed clade-specific sequence recruitment patterns across diverse terrestrial soil metagenomes. Additionally, sorted-MAGs expanded the rare biosphere not captured through MAGs from bulk sequences, exemplified through phylogenetic and functional analyses of members of the phylum Bacteroidetes. Analysis of 67 Bacteroidetes sorted-MAGs showed conserved patterns of carbon metabolism across four clades. These results indicate that mini-metagenomics enables genome-resolved investigation of predicted metabolism and demonstrates the utility of combining metagenomics methods to tap into the diversity of heterogeneous microbial assemblages.

          IMPORTANCE Microbial ecologists have historically used cultivation-based approaches as well as amplicon sequencing and shotgun metagenomics to characterize microbial diversity in soil. However, challenges persist in the study of microbial diversity, including the recalcitrance of the majority of microorganisms to laboratory cultivation and limited sequence assembly from highly complex samples. The uncultivated majority thus remains a reservoir of untapped genetic diversity. To address some of the challenges associated with bulk metagenomics as well as low throughput of single-cell genomics, we applied flow cytometry-enabled mini-metagenomics to capture expanded microbial diversity from forest soil and compare it to soil bulk metagenomics. Our resulting data from this pooled-cell sorting approach combined with bulk metagenomics revealed increased phylogenetic diversity through novel soil taxa and rare biosphere members. In-depth analysis of genomes within the highly represented Bacteroidetes phylum provided insights into conserved and clade-specific patterns of carbon metabolism.

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          Most cited references 61

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          Extreme genome reduction in symbiotic bacteria.

          Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.
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            Soil warming and carbon-cycle feedbacks to the climate system.

            In a decade-long soil warming experiment in a mid-latitude hardwood forest, we documented changes in soil carbon and nitrogen cycling in order to investigate the consequences of these changes for the climate system. Here we show that whereas soil warming accelerates soil organic matter decay and carbon dioxide fluxes to the atmosphere, this response is small and short-lived for a mid-latitude forest, because of the limited size of the labile soil carbon pool. We also show that warming increases the availability of mineral nitrogen to plants. Because plant growth in many mid-latitude forests is nitrogen-limited, warming has the potential to indirectly stimulate enough carbon storage in plants to at least compensate for the carbon losses from soils. Our results challenge assumptions made in some climate models that lead to projections of large long-term releases of soil carbon in response to warming of forest ecosystems.
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              Microbial diversity and function in soil: from genes to ecosystems.

              Soils sustain an immense diversity of microbes, which, to a large extent, remains unexplored. A range of novel methods, most of which are based on rRNA and rDNA analyses, have uncovered part of the soil microbial diversity. The next step in the era of microbial ecology is to extract genomic, evolutionary and functional information from bacterial artificial chromosome libraries of the soil community genomes (the metagenome). Sophisticated analyses that apply molecular phylogenetics, DNA microarrays, functional genomics and in situ activity measurements will provide huge amounts of new data, potentially increasing our understanding of the structure and function of soil microbial ecosystems, and the interactions that occur within them. This review summarizes the recent progress in studies of soil microbial communities with focus on novel methods and approaches that provide new insight into the relationship between phylogenetic and functional diversity.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                10 March 2020
                Mar-Apr 2020
                : 5
                : 2
                Affiliations
                [a ]Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts Amherst, Amherst, Massachusetts, USA
                [b ]Department of Energy, Joint Genome Institute, Berkeley, California, USA
                [c ]Centre for Microbiology and Environmental Systems Science, Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Vienna, Austria
                [d ]Department of Biological Sciences, Smith College, Northampton, Massachusetts, USA
                [e ]Department of Biology, University of Massachusetts Amherst, Amherst, Massachusetts, USA
                Pacific Northwest National Laboratory
                Author notes
                Address correspondence to T. Woyke, twoyke@ 123456lbl.gov .

                Citation Alteio LV, Schulz F, Seshadri R, Varghese N, Rodriguez-Reillo W, Ryan E, Goudeau D, Eichorst SA, Malmstrom RR, Bowers RM, Katz LA, Blanchard JL, Woyke T. 2020. Complementary metagenomic approaches improve reconstruction of microbial diversity in a forest soil. mSystems 5:e00768-19. https://doi.org/10.1128/mSystems.00768-19.

                Article
                mSystems00768-19
                10.1128/mSystems.00768-19
                7065516
                32156798
                Copyright © 2020 Alteio et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Page count
                supplementary-material: 10, Figures: 5, Tables: 0, Equations: 0, References: 105, Pages: 18, Words: 12682
                Product
                Funding
                Funded by: U.S. Department of Energy (DOE), https://doi.org/10.13039/100000015;
                Award ID: DE-AC02-05CH11231
                Award Recipient : Award Recipient : Award Recipient : Award Recipient : Award Recipient : Award Recipient : Award Recipient : Award Recipient :
                Funded by: Austrian Science Fund (FWF), https://doi.org/10.13039/501100002428;
                Award ID: P26392-B20
                Award Recipient :
                Funded by: MoSTR | National Science Foundation (NSF), https://doi.org/10.13039/501100008982;
                Award ID: DEB 1237491
                Award ID: DEB 1456528
                Award Recipient : Award Recipient : Award Recipient :
                Categories
                Research Article
                Ecological and Evolutionary Science
                Custom metadata
                March/April 2020

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