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UC Davis UC Davis Previously Published Works UC Davis UC Davis Previously Published Works Title New Biological Insights Into How Deforestation in Amazonia Affects Soil Microbial Communities Using Metagenomics and Metagenome-Assembled Genomes. Permalink https://escholarship.org/uc/item/8032c1dz Journal Frontiers in microbiology, 9(JUL) ISSN 1664-302X Authors Kroeger, Marie E Delmont, Tom O Eren, AM et al. Publication Date 2018 DOI 10.3389/fmicb.2018.01635 Peer reviewed eScholarship.org Powered by the California Digital Library University of California fmicb-09-01635 July 20, 2018 Time: 14:55 # 1 ORIGINAL RESEARCH published: 23 July 2018 doi: 10.3389/fmicb.2018.01635 New Biological Insights Into How Deforestation in Amazonia Affects Soil Microbial Communities Using Metagenomics and Metagenome-Assembled Genomes Marie E. Kroeger1, Tom O. Delmont2, A. M. Eren2,3, Kyle M. Meyer4, Jiarong Guo5, Kiran Khan1, Jorge L. M. Rodrigues6, Brendan J. M. Bohannan4, Susannah G. Tringe7, Clovis D. Borges8, James M. Tiedje5, Siu M. Tsai8 and Klaus Nüsslein1* Edited by: 1 Department of Microbiology, University of Massachusetts Amherst, Amherst, MA, United States, 2 Department of Medicine, Etienne Yergeau, University of Chicago, Chicago, IL, United States, 3 Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, Institut National de la Recheriche MA, United States, 4 Institute of Ecology and Evolution, University of Oregon, Eugene, OR, United States, 5 Center Scientifique (INRS), Canada for Microbial Ecology, Michigan State University, East Lansing, MI, United States, 6 Department of Land, Air, and Water 7 Reviewed by: Resources, University of California, Davis, Davis, CA, United States, DOE Joint Genome Institute, Walnut Creek, CA, 8 Carl-Eric Wegner, United States, Centro de Energia Nuclear na Agricultura, University of São Paulo, Piracicaba, Brazil Friedrich-Schiller-Universität Jena, Germany Deforestation in the Brazilian Amazon occurs at an alarming rate, which has broad Terrence H. Bell, Pennsylvania State University, effects on global greenhouse gas emissions, carbon storage, and biogeochemical United States cycles. In this study, soil metagenomes and metagenome-assembled genomes (MAGs) Erick Cardenas Poire, Microbiome Insights, Canada were analyzed for alterations to microbial community composition, functional groups, *Correspondence: and putative physiology as it related to land-use change and tropical soil. A total Klaus Nüsslein of 28 MAGs were assembled encompassing 10 phyla, including both dominant [email protected] and rare biosphere lineages. Amazon Acidobacteria subdivision 3, Melainabacteria, Specialty section: Microgenomates, and Parcubacteria were found exclusively in pasture soil samples, This article was submitted to while Candidatus Rokubacteria was predominant in the adjacent rainforest soil. These Terrestrial Microbiology, a section of the journal shifts in relative abundance between land-use types were supported by the different Frontiers in Microbiology putative physiologies and life strategies employed by the taxa. This research provides Received: 16 April 2018 unique biological insights into candidate phyla in tropical soil and how deforestation may Accepted: 30 June 2018 impact the carbon cycle and affect climate change. Published: 23 July 2018 Citation: Keywords: Amazon rainforest soil, land-use change, metagenome assembled genomes, rare biosphere, soil Kroeger ME, Delmont TO, Eren AM, metagenomics Meyer KM, Guo J, Khan K, Rodrigues JLM, Bohannan BJM, Tringe SG, Borges CD, Tiedje JM, INTRODUCTION Tsai SM and Nüsslein K (2018) New Biological Insights Into How The Amazon Basin contains the largest continuous tropical rainforest on the planet (Laurance Deforestation in Amazonia Affects Soil et al., 2001) and is home to unparalleled levels of plant and animal diversity (Da Silva et al., Microbial Communities Using 2005). Rainforests in this region are under threat from human activities, with the largest single Metagenomics and Metagenome-Assembled threat being conversion to agriculture (Soares-Filho et al., 2006). Several studies have illustrated Genomes. Front. Microbiol. 9:1635. that human activities in the tropics such as land use change have adverse effects on macro- doi: 10.3389/fmicb.2018.01635 organismal biodiversity (Dale et al., 1994; McKinney and Lockwood, 1999; Sala et al., 2000), and Frontiers in Microbiology| www.frontiersin.org 1 July 2018| Volume 9| Article 1635 fmicb-09-01635 July 20, 2018 Time: 14:55 # 2 Kroeger et al. Deforestation Affects Amazonian Soil Microbes more recently it became apparent that belowground microbial performed genome-resolved metagenomics on soil and among communities are altered as well (Rodrigues et al., 2013; Paula those, some have perturbed the community composition prior to et al., 2014; Ranjan et al., 2015; Meyer et al., 2017). Soil sampling to lower the complexity of the microbial communities microbial biodiversity in the Amazonian tropics is primarily (Delmont et al., 2015; Yeoh et al., 2015), while others have known through 16S rRNA and ITS gene sequencing surveys assembled MAGs without manipulation (Butterfield et al., 2016; (Borneman and Triplett, 1997; Peixoto et al., 2002; Jesus et al., White et al., 2016; Tas et al., 2018). Despite these recent 2009; Tripathi et al., 2012; Mueller et al., 2014), with only limited metagenomic accomplishments, the genomic content of most genomic and metagenomic surveys (Navarrete et al., 2015; Meyer microbial populations inhabiting soil from the Amazon basin and et al., 2017). elsewhere have yet to be characterized. Phylogenetic analyses based on 16S rRNA gene sequences Here, we analyzed ten extensive tropical soil metagenomes organize bacterial and archaeal life into more than 60 phyla. (five from pristine rainforest soil and five from an adjacent cattle Half of these phyla have no cultured representatives, yet these pasture) to understand the microbial community composition ‘candidate’ phyla represent a substantial portion of the tree of and how deforestation may affect these communities. In life (Hugenholtz, 2002; Rinke et al., 2013; Hug et al., 2016). addition, we also characterized 28 MAGs from the rare Until recently, these microorganisms have only been detected soil biosphere for their functional potential in these tropical through surveys of 16S rRNA gene surveys of environmental rainforest soils, because there is no knowledge of the metabolic sequencing (Dojka et al., 2000; Hedlund et al., 2014), which capabilities of these groups either in any soil (Microgenomates provided very little direct information about their ecology and Parcubacteria) or in tropical soils (Rokubacteria). We or metabolic capabilities. With the development of shotgun also described shifts in the soil chemistry, and in the soil metagenomics, insights into the diversity and functional potential microbial functional potential. The sequencing depth of our of microbial communities have drastically increased. Expanding dataset (6.4 billion shotgun metagenomic reads) was critical in on that advance, genome-resolved metagenomics (Alneberg et al., the successful reconstruction of microbial genomes from this 2014; Imelfort et al., 2014; Eren et al., 2015; Kang et al., 2015; highly complex biological system. We were able to characterize Sangwan et al., 2016) and single-cell genome sequencing (Gawad MAGs encompassing 10 phyla, including CPR superphyla et al., 2016) were developed, and can now be used to characterize Microgenomates, and Parcubacteria, and from ubiquitous soil the genomic content of microbial populations without the need bacteria, Acidobacteria. Using comparative genomic approaches, for cultivation. Metagenome-assembled genomes (MAGs) have we elucidated the unique features and potential metabolic been characterized from a variety of environments, including capabilities of various tropical soil microbial populations. recently from soil (Wrighton et al., 2012; Brown et al., 2015; Not only does our study begin to depict the genomic and Delmont et al., 2015; Sekiguchi et al., 2015; Butterfield et al., functional potential of poorly understood phyla, but it also 2016; Hu et al., 2016; White et al., 2016). By integrating increases our understanding of understudied tropical microbial large sequencing datasets from environmental samples into biodiversity. reconstructed genomic composition, MAGs have increased the resolution at which microbial ecologists can understand a microorganism’s functional potential. MATERIALS AND METHODS The use of MAGs has increased our understanding of candidate phyla in the environment (Siegl et al., 2011; Wrighton Site Description, Sampling, and Soil et al., 2012; Kantor et al., 2013; McLean et al., 2013; Probst Chemistry et al., 2017). A study by Brown et al.(2015) identified a This study was performed at the Amazon Rainforest Microbial distinct radiation from known bacteria that altered our view of Observatory site, established in 2009 (10◦100500 S and 62◦4902700 the tree of life and was termed the candidate phyla radiation W). Sample design and soil chemical analyses were performed (CPR) (Hug et al., 2016). Altogether, the CPR lineages might as specified previously (Rodrigues et al., 2013; Meyer et al., encompass over 70 phyla and two superphyla, Microgenomates, 2017). Briefly, in April 2010 soil cores collected from primary and Parcubacteria (Anantharaman et al., 2016). CPR genomes rainforest and a 38-year-old converted pasture (five each). The are generally streamlined (<1.5 Mb) with limited biosynthetic pasture site was initially a pristine rainforest.
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