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Title: Landscape topography structures the soil microbiome in arctic polygonal tundra

Abstract

In the Arctic, environmental factors governing microbial degradation of soil carbon (C) in active layer and permafrost are poorly understood. Here we determined the functional potential of soil microbiomes horizontally and vertically across a cryoperturbed polygonal landscape in Alaska. With comparative metagenomics, genome binning of novel microbes, and gas flux measurements we show that microbial greenhouse gas (GHG) production is strongly correlated to landscape topography. Active layer and permafrost harbor contrasting microbiomes, with increasing amounts of Actinobacteria correlating with decreasing soil C in permafrost. While microbial functions such as fermentation and methanogenesis were dominant in wetter polygons, in drier polygons genes for C mineralization and CH 4 oxidation were abundant. The active layer microbiome was poised to assimilate N and not to release N 2 O, reflecting low N 2 O flux measurements. These results provide mechanistic links of microbial metabolism to GHG fluxes that are needed for the refinement of model predictions.

Authors:
 [1];  [1]; ORCiD logo [1];  [1];  [1];  [1]; ORCiD logo [2];  [3];  [1];  [4]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1423412
Alternate Identifier(s):
OSTI ID: 1433134
Report Number(s):
PNNL-SA-126595
Journal ID: ISSN 2041-1723
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; soil microbiome; metagenome; polygonal tundra; greenhouse gas

Citation Formats

Taş, Neslihan, Prestat, Emmanuel, Wang, Shi, Wu, Yuxin, Ulrich, Craig, Kneafsey, Timothy, Tringe, Susannah G., Torn, Margaret S., Hubbard, Susan S., and Jansson, Janet K. Landscape topography structures the soil microbiome in arctic polygonal tundra. United States: N. p., 2018. Web. doi:10.1038/s41467-018-03089-z.
Taş, Neslihan, Prestat, Emmanuel, Wang, Shi, Wu, Yuxin, Ulrich, Craig, Kneafsey, Timothy, Tringe, Susannah G., Torn, Margaret S., Hubbard, Susan S., & Jansson, Janet K. Landscape topography structures the soil microbiome in arctic polygonal tundra. United States. https://doi.org/10.1038/s41467-018-03089-z
Taş, Neslihan, Prestat, Emmanuel, Wang, Shi, Wu, Yuxin, Ulrich, Craig, Kneafsey, Timothy, Tringe, Susannah G., Torn, Margaret S., Hubbard, Susan S., and Jansson, Janet K. Thu . "Landscape topography structures the soil microbiome in arctic polygonal tundra". United States. https://doi.org/10.1038/s41467-018-03089-z. https://www.osti.gov/servlets/purl/1423412.
@article{osti_1423412,
title = {Landscape topography structures the soil microbiome in arctic polygonal tundra},
author = {Taş, Neslihan and Prestat, Emmanuel and Wang, Shi and Wu, Yuxin and Ulrich, Craig and Kneafsey, Timothy and Tringe, Susannah G. and Torn, Margaret S. and Hubbard, Susan S. and Jansson, Janet K.},
abstractNote = {In the Arctic, environmental factors governing microbial degradation of soil carbon (C) in active layer and permafrost are poorly understood. Here we determined the functional potential of soil microbiomes horizontally and vertically across a cryoperturbed polygonal landscape in Alaska. With comparative metagenomics, genome binning of novel microbes, and gas flux measurements we show that microbial greenhouse gas (GHG) production is strongly correlated to landscape topography. Active layer and permafrost harbor contrasting microbiomes, with increasing amounts of Actinobacteria correlating with decreasing soil C in permafrost. While microbial functions such as fermentation and methanogenesis were dominant in wetter polygons, in drier polygons genes for C mineralization and CH 4 oxidation were abundant. The active layer microbiome was poised to assimilate N and not to release N 2 O, reflecting low N 2 O flux measurements. These results provide mechanistic links of microbial metabolism to GHG fluxes that are needed for the refinement of model predictions.},
doi = {10.1038/s41467-018-03089-z},
journal = {Nature Communications},
number = 1,
volume = 9,
place = {United States},
year = {Thu Feb 22 00:00:00 EST 2018},
month = {Thu Feb 22 00:00:00 EST 2018}
}

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Cited by: 58 works
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Works referenced in this record:

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Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest
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Pan-Arctic ice-wedge degradation in warming permafrost and its influence on tundra hydrology
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Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
journal, April 2015

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  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
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Permafrost thaw and resulting soil moisture changes regulate projected high-latitude CO 2 and CH 4 emissions
journal, September 2015


Effects of thermo-erosion gullying on hydrologic flow networks, discharge and soil loss
journal, October 2014


Effect of permafrost thaw on CO 2 and CH 4 exchange in a western Alaska peatland chronosequence
journal, August 2014

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  • Environmental Research Letters, Vol. 9, Issue 8
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The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013

  • Overbeek, Ross; Olson, Robert; Pusch, Gordon D.
  • Nucleic Acids Research, Vol. 42, Issue D1
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FOAM (Functional Ontology Assignments for Metagenomes): a Hidden Markov Model (HMM) database with environmental focus
journal, September 2014

  • Prestat, Emmanuel; David, Maude M.; Hultman, Jenni
  • Nucleic Acids Research, Vol. 42, Issue 19
  • DOI: 10.1093/nar/gku702

Methanolinea tarda gen. nov., sp. nov., a methane-producing archaeon isolated from a methanogenic digester sludge
journal, January 2008

  • Imachi, H.; Sakai, S.; Sekiguchi, Y.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 1
  • DOI: 10.1099/ijs.0.65394-0

Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage 'Rice Cluster I', and proposal of the new archaeal order Methanocellales ord. nov.
journal, April 2008

  • Sakai, S.; Imachi, H.; Hanada, S.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 4
  • DOI: 10.1099/ijs.0.65571-0

Stoichiometry and temperature sensitivity of methanogenesis and CO 2 production from saturated polygonal tundra in Barrow, Alaska
journal, November 2014

  • Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J.
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Isotopic insights into methane production, oxidation, and emissions in Arctic polygon tundra
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Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra: WARMING OF ALASKAN TUNDRA
journal, February 2011


Bacterial quorum sensing and nitrogen cycling in rhizosphere soil: Bacterial QS and rhizosphere nitrogen cycling
journal, November 2008


Methane-cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes
journal, March 2012


Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils
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The deep cold biosphere: facts and hypothesis
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Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation
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Geophysical estimation of shallow permafrost distribution and properties in an ice-wedge polygon-dominated Arctic tundra region
journal, January 2016


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


Metagenomic Insights into Anaerobic Metabolism along an Arctic Peat Soil Profile
journal, May 2013


Demonstrating microbial co-occurrence pattern analyses within and between ecosystems
journal, July 2014


Recent trends and drivers of regional sources and sinks of carbon dioxide
journal, January 2015


Works referencing / citing this record:

Understanding spatial variability of methane fluxes in Arctic wetlands through footprint modelling
journal, December 2019

  • Reuss-Schmidt, Kassandra; Levy, Peter; Oechel, Walter
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The known and the unknown in soil microbial ecology
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Distinct Taxonomic and Functional Profiles of the Microbiome Associated With Different Soil Horizons of a Moist Tussock Tundra in Alaska
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Microbial community composition and abundance after millennia of submarine permafrost warming
journal, January 2019

  • Mitzscherling, Julia; Horn, Fabian; Winterfeld, Maria
  • Biogeosciences, Vol. 16, Issue 19
  • DOI: 10.5194/bg-16-3941-2019

Nutrient Release From Permafrost Thaw Enhances CH 4 Emissions From Arctic Tundra Wetlands
journal, June 2019

  • Lara, Mark J.; Lin, David H.; Andresen, Christian
  • Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 6
  • DOI: 10.1029/2018jg004641

Mechanistic Modeling of Microtopographic Impacts on CO 2 and CH 4 Fluxes in an Alaskan Tundra Ecosystem Using the CLM‐Microbe Model
journal, December 2019

  • Wang, Yihui; Yuan, Fengming; Yuan, Fenghui
  • Journal of Advances in Modeling Earth Systems, Vol. 11, Issue 12
  • DOI: 10.1029/2019ms001771

Tundra microbial community taxa and traits predict decomposition parameters of stable, old soil organic carbon
journal, August 2019


Climate change microbiology — problems and perspectives
journal, May 2019

  • Hutchins, David A.; Jansson, Janet K.; Remais, Justin V.
  • Nature Reviews Microbiology, Vol. 17, Issue 6
  • DOI: 10.1038/s41579-019-0178-5

Genome-centric view of carbon processing in thawing permafrost
journal, July 2018


Denitrifiers, nitrogen-fixing bacteria and N2O soil gas flux in high Arctic ice-wedge polygon cryosols
journal, April 2019

  • Altshuler, Ianina; Ronholm, Jennifer; Layton, Alice
  • FEMS Microbiology Ecology, Vol. 95, Issue 5
  • DOI: 10.1093/femsec/fiz049

Prokaryotic community shifts during soil formation on sands in the tundra zone
journal, April 2019


Bacterial and Archaeal Metagenome-Assembled Genome Sequences from Svalbard Permafrost
journal, July 2019

  • Xue, Yaxin; Jonassen, Inge; Øvreås, Lise
  • Microbiology Resource Announcements, Vol. 8, Issue 27
  • DOI: 10.1128/mra.00516-19

Prokaryotic community shifts during soil formation on sands in the tundra zone
journal, April 2019