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      Cellulose-Enriched Microbial Communities from Leaf-Cutter Ant ( Atta colombica) Refuse Dumps Vary in Taxonomic Composition and Degradation Ability

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          Abstract

          Deconstruction of the cellulose in plant cell walls is critical for carbon flow through ecosystems and for the production of sustainable cellulosic biofuels. Our understanding of cellulose deconstruction is largely limited to the study of microbes in isolation, but in nature, this process is driven by microbes within complex communities. In Neotropical forests, microbes in leaf-cutter ant refuse dumps are important for carbon turnover. These dumps consist of decaying plant material and a diverse bacterial community, as shown here by electron microscopy. To study the portion of the community capable of cellulose degradation, we performed enrichments on cellulose using material from five Atta colombica refuse dumps. The ability of enriched communities to degrade cellulose varied significantly across refuse dumps. 16S rRNA gene amplicon sequencing of enriched samples identified that the community structure correlated with refuse dump and with degradation ability. Overall, samples were dominated by Bacteroidetes, Gammaproteobacteria, and Betaproteobacteria. Half of abundant operational taxonomic units (OTUs) across samples were classified within genera containing known cellulose degraders, including Acidovorax, the most abundant OTU detected across samples, which was positively correlated with cellulolytic ability. A representative Acidovorax strain was isolated, but did not grow on cellulose alone. Phenotypic and compositional analyses of enrichment cultures, such as those presented here, help link community composition with cellulolytic ability and provide insight into the complexity of community-based cellulose degradation.

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          Most cited references33

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          The diversity and biogeography of soil bacterial communities.

          For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.
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            Fast UniFrac: Facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data

            Next-generation sequencing techniques, and PhyloChip, have made simultaneous phylogenetic analyses of hundreds of microbial communities possible. Insight into community structure has been limited by the inability to integrate and visualize such vast datasets. Fast UniFrac overcomes these issues, allowing integration of larger numbers of sequences and samples into a single analysis. Its new array-based implementation offers orders of magnitude improvements over the original version. New 3D visualization of principal coordinates analysis (PCoA) results, with the option to view multiple coordinate axes simultaneously, provides a powerful way to quickly identify patterns that relate vast numbers of microbial communities. We demonstrate the potential of Fast UniFrac using examples from three data types: Sanger-sequencing studies of diverse free-living and animal-associated bacterial assemblages and from the gut of obese humans as they diet, pyrosequencing data integrated from studies of the human hand and gut, and PhyloChip data from a study of citrus pathogens. We show that a Fast UniFrac analysis using a reference tree recaptures patterns that could not be detected without considering phylogenetic relationships and that Fast UniFrac, coupled with BLAST-based sequence assignment, can be used to quickly analyze pyrosequencing runs containing hundreds of thousands of sequences, revealing patterns relating human and gut samples. Finally, we show that the application of Fast UniFrac to PhyloChip data could identify well-defined subcategories associated with infection. Together, these case studies point the way towards a broad range of applications and demonstrate some of the new features of Fast UniFrac.
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              Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina).

              Trichoderma reesei is the main industrial source of cellulases and hemicellulases used to depolymerize biomass to simple sugars that are converted to chemical intermediates and biofuels, such as ethanol. We assembled 89 scaffolds (sets of ordered and oriented contigs) to generate 34 Mbp of nearly contiguous T. reesei genome sequence comprising 9,129 predicted gene models. Unexpectedly, considering the industrial utility and effectiveness of the carbohydrate-active enzymes of T. reesei, its genome encodes fewer cellulases and hemicellulases than any other sequenced fungus able to hydrolyze plant cell wall polysaccharides. Many T. reesei genes encoding carbohydrate-active enzymes are distributed nonrandomly in clusters that lie between regions of synteny with other Sordariomycetes. Numerous genes encoding biosynthetic pathways for secondary metabolites may promote survival of T. reesei in its competitive soil habitat, but genome analysis provided little mechanistic insight into its extraordinary capacity for protein secretion. Our analysis, coupled with the genome sequence data, provides a roadmap for constructing enhanced T. reesei strains for industrial applications such as biofuel production.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 March 2016
                2016
                : 11
                : 3
                : e0151840
                Affiliations
                [1 ]Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America
                [2 ]Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America
                [3 ]Centro de Investigación en Estructuras Microscópicas, Universidad de Costa Rica, San José, Costa Rica
                [4 ]Centro de Investigación en Enfermedades Tropicales, Universidad de Costa Rica, San José, Costa Rica
                [5 ]Departamento de Bioquímica, Facultad de Medicina, Universidad de Costa Rica, San José, Costa Rica
                [6 ]Centro de Investigación en Biología Celular y Molecular, Universidad de Costa Rica, San José, Costa Rica
                University Paris South, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GRL ALJ RDMS AJB AAPT CRC. Performed the experiments: GRL ALJ RDMS KP HAH. Analyzed the data: GRL ALJ RDMS. Wrote the paper: GRL RDMS AJB CRC.

                Article
                PONE-D-15-53463
                10.1371/journal.pone.0151840
                4801328
                26999749
                037c3d28-f129-40a2-a3b7-5f180d0938e3
                © 2016 Lewin et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 December 2015
                : 5 March 2016
                Page count
                Figures: 6, Tables: 2, Pages: 22
                Funding
                This work was supported by the Great Lakes Bioenergy Research Center [Department of Energy, Office of Science, Biological and Environmental Research DE-FC02-07ER64494, http://science.energy.gov/ber/]; the National Science Foundation [DGE-1256259 to GRL, DEB-0747002, and MCB-0702025, http://www.nsf.gov/]; the National Institutes of Health [National Research Service Award T32 GM07215, http://www.nih.gov/]; the UW-Madison's Hilldale Undergraduate/Faculty Research Fellowship to ALJ and CRC [ http://awards.advising.wisc.edu/hilldale-undergraduatefaculty-research-fellowship/]; and support from the University of Costa Rica [ http://www.ucr.ac.cr/] and the Costa Rican Ministry of Science and Technology [ https://www.micit.go.cr/] to RDMS and AAPT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Cellulose
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Cellulose
                Engineering and Technology
                Equipment
                Laboratory Equipment
                Filter Paper
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Ants
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                Non-coding RNA
                Ribosomal RNA
                Biology and life sciences
                Biochemistry
                Ribosomes
                Ribosomal RNA
                Biology and life sciences
                Cell biology
                Cellular structures and organelles
                Ribosomes
                Ribosomal RNA
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Sequencing Techniques
                Sequence Analysis
                Sequence Databases
                Research and Analysis Methods
                Molecular Biology Techniques
                Sequencing Techniques
                Sequence Analysis
                Sequence Databases
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Organisms
                Bacteria
                Biology and Life Sciences
                Ecology
                Community Ecology
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Custom metadata
                Amplicon sequencing data are available using Sequence Read Archive accession number SRP059774, and the 16S rRNA gene sequence for strain Acidovorax sp. AcolKP-3D is available in GenBank using accession number KT150251. All other relevant data are within this paper and its Supporting Information files.

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