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Title: Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil

Abstract

Here, we explored microbial contributions to decomposition using a sophisticated approach to DNA Stable Isotope Probing (SIP). Our experiment evaluated the dynamics and ecological characteristics of functionally defined microbial groups that metabolize labile and structural C in soils. We added to soil a complex amendment representing plant derived organic matter substituted with either 13C-xylose or 13C-cellulose to represent labile and structural C pools derived from abundant components of plant biomass. We also found evidence for 13C-incorporation into DNA from 13C-xylose and 13C-cellulose in 49 and 63 operational taxonomic units (OTUs), respectively. The types of microorganisms that assimilated 13C in the 13C-xylose treatment changed over time being predominantly Firmicutes at day 1 followed by Bacteroidetes at day 3 and then Actinobacteria at day 7. Furthermore, these 13C-labeling dynamics suggest labile C traveled through different trophic levels. In contrast, microorganisms generally metabolized cellulose-C after 14 days and did not change to the same extent in phylogenetic composition over time. Microorganisms that metabolized cellulose-C belonged to poorly characterized but cosmopolitan soil lineages including Verrucomicrobia, Chloroflexi, and Planctomycetes.

Authors:
 [1];  [1];  [1];  [2];  [1]
  1. Cornell Univ., Ithaca, NY (United States)
  2. Butler Univ., Indianapolis, IN (United States)
Publication Date:
Research Org.:
Cornell Univ., Ithaca, NY (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1864330
Alternate Identifier(s):
OSTI ID: 1282112; OSTI ID: 1343031
Report Number(s):
LLNL-JRNL-675821
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
SC0016364; SC0004486; SC0010558; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; stable isotope probing; carbon cycle; decomposition; verrucomicrobia; cellulose; soil; trophic; DNA-SIP; dna-sip; microbial community composition; 16s ribosomal-rna; functional-significance; labile carbon; climate-change; bulk soil; bacterial; diversity; nitrogen; tools; 54 ENVIRONMENTAL SCIENCES; stable isotopeprobing; soil trophic

Citation Formats

Pepe-Ranney, Charles, Campbell, Ashley N., Koechli, Chantal N., Berthrong, Sean, and Buckley, Daniel H. Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00703.
Pepe-Ranney, Charles, Campbell, Ashley N., Koechli, Chantal N., Berthrong, Sean, & Buckley, Daniel H. Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil. United States. https://doi.org/10.3389/fmicb.2016.00703
Pepe-Ranney, Charles, Campbell, Ashley N., Koechli, Chantal N., Berthrong, Sean, and Buckley, Daniel H. Thu . "Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil". United States. https://doi.org/10.3389/fmicb.2016.00703. https://www.osti.gov/servlets/purl/1864330.
@article{osti_1864330,
title = {Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil},
author = {Pepe-Ranney, Charles and Campbell, Ashley N. and Koechli, Chantal N. and Berthrong, Sean and Buckley, Daniel H.},
abstractNote = {Here, we explored microbial contributions to decomposition using a sophisticated approach to DNA Stable Isotope Probing (SIP). Our experiment evaluated the dynamics and ecological characteristics of functionally defined microbial groups that metabolize labile and structural C in soils. We added to soil a complex amendment representing plant derived organic matter substituted with either 13C-xylose or 13C-cellulose to represent labile and structural C pools derived from abundant components of plant biomass. We also found evidence for 13C-incorporation into DNA from 13C-xylose and 13C-cellulose in 49 and 63 operational taxonomic units (OTUs), respectively. The types of microorganisms that assimilated 13C in the 13C-xylose treatment changed over time being predominantly Firmicutes at day 1 followed by Bacteroidetes at day 3 and then Actinobacteria at day 7. Furthermore, these 13C-labeling dynamics suggest labile C traveled through different trophic levels. In contrast, microorganisms generally metabolized cellulose-C after 14 days and did not change to the same extent in phylogenetic composition over time. Microorganisms that metabolized cellulose-C belonged to poorly characterized but cosmopolitan soil lineages including Verrucomicrobia, Chloroflexi, and Planctomycetes.},
doi = {10.3389/fmicb.2016.00703},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Thu May 12 00:00:00 EDT 2016},
month = {Thu May 12 00:00:00 EDT 2016}
}

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Picante: R tools for integrating phylogenies and ecology
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adephylo: new tools for investigating the phylogenetic signal in biological traits
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Search and clustering orders of magnitude faster than BLAST
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Infernal 1.1: 100-fold faster RNA homology searches
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NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes
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The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
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Kallotenue papyrolyticum gen. nov., sp. nov., a cellulolytic and filamentous thermophile that represents a novel lineage (Kallotenuales ord. nov., Kallotenuaceae fam. nov.) within the class Chloroflexia
journal, August 2013

  • Cole, J. K.; Gieler, B. A.; Heisler, D. L.
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Climate change alters ecological strategies of soil bacteria
journal, November 2013

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  • DOI: 10.1111/ele.12206

Microbial community dynamics alleviate stoichiometric constraints during litter decay
journal, March 2014

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Total carbon and nitrogen in the soils of the world
journal, June 1996


Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils
journal, December 2008


Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen: Metabolic response of soil cellulose degraders
journal, December 2009


Environmental factors influencing the distribution of rRNA from Verrucomicrobia in soil
journal, March 2001


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journal, November 2007


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journal, October 2013


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Arthropod Regulation of Micro- and Mesobiota in Below-Ground Detrital Food Webs
journal, January 1988


BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Incorporating 16S Gene Copy Number Information Improves Estimates of Microbial Diversity and Abundance
journal, October 2012


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Testing the functional significance of microbial community composition
journal, February 2009

  • Strickland, Michael S.; Lauber, Christian; Fierer, Noah
  • Ecology, Vol. 90, Issue 2
  • DOI: 10.1890/08-0296.1

Aerobic and Anaerobic Microbial Populations in No-till and Plowed Soils
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