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Title: NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient

Abstract

Since nitrogen (N) is often limiting in permafrost soils, we investigated the N2-fixing genetic potential and the inferred taxa harboring those genes by sequencing nifH gene fragments in samples taken along a permafrost thaw gradient in an Alaskan boreal soil. Samples from minimally, moderately and extensively thawed sites were taken to a depth of 79 cm to encompass zones above and below the depth of the water table. NifH reads were translated with frameshift correction and 112,476 sequences were clustered at 5% amino acid dissimilarity resulting in 1,631 OTUs. Sample depth in relation to water table depth was correlated to differences in the NifH sequence classes with those most closely related to group I nifH-harboring Alpha- and Beta-Proteobacteria in higher abundance above water table depth while those related to group III nifH-harboring Delta Proteobacteria more abundant below. The most dominant below water table depth NifH sequences, comprising 1/3 of the total, were distantly related to Verrucomicrobia-Opitutaceae. Overall, these results suggest that permafrost thaw alters the class-level composition of N2-fixing communities in the thawed soil layers and that this distinction corresponds to the depth of the water table. These nifH data were also compared to nifH sequences obtained from a studymore » at an Alaskan taiga site, and to those of other geographically distant, non-permafrost sites. The two Alaska sites were differentiated largely by changes in relative abundances of the same OTUs, whereas the non-Alaska sites were differentiated by the lack of many Alaskan OTUs, and the presence of unique halophilic, sulfate- and iron-reducing taxa in the Alaska sites.« less

Authors:
 [1];  [2];  [3];  [4];  [3];  [3];  [3];  [3];  [3];  [5];  [6];  [4];  [7]
  1. Arizona State Univ., Mesa, AZ (United States); Arizona State Univ., Tempe, AZ (United States)
  2. Univ. of Oklahoma, Norman, OK (United States); Xiamen Univ., Xiamen (China)
  3. Univ. of Oklahoma, Norman, OK (United States)
  4. Michigan State Univ., East Lansing, MI (United States)
  5. Xiamen Univ., Xiamen (China)
  6. Northern Arizona Univ., Flagstaff, AZ (United States)
  7. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1379591
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal Issue: NOV; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; nifH; nitrogen-fixing; permafrost; diazotroph; nitrogen; microbial

Citation Formats

Penton, C. Ryan, Yang, Caiyun, Wu, Liyou, Wang, Qiong, Zhang, Jin, Liu, Feifei, Qin, Yujia, Deng, Ye, Hemme, Christopher L., Zheng, Tianling, Schuur, Edward A. G., Tiedje, James, and Zhou, Jizhong. NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.01894.
Penton, C. Ryan, Yang, Caiyun, Wu, Liyou, Wang, Qiong, Zhang, Jin, Liu, Feifei, Qin, Yujia, Deng, Ye, Hemme, Christopher L., Zheng, Tianling, Schuur, Edward A. G., Tiedje, James, & Zhou, Jizhong. NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient. United States. https://doi.org/10.3389/fmicb.2016.01894
Penton, C. Ryan, Yang, Caiyun, Wu, Liyou, Wang, Qiong, Zhang, Jin, Liu, Feifei, Qin, Yujia, Deng, Ye, Hemme, Christopher L., Zheng, Tianling, Schuur, Edward A. G., Tiedje, James, and Zhou, Jizhong. Thu . "NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient". United States. https://doi.org/10.3389/fmicb.2016.01894. https://www.osti.gov/servlets/purl/1379591.
@article{osti_1379591,
title = {NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient},
author = {Penton, C. Ryan and Yang, Caiyun and Wu, Liyou and Wang, Qiong and Zhang, Jin and Liu, Feifei and Qin, Yujia and Deng, Ye and Hemme, Christopher L. and Zheng, Tianling and Schuur, Edward A. G. and Tiedje, James and Zhou, Jizhong},
abstractNote = {Since nitrogen (N) is often limiting in permafrost soils, we investigated the N2-fixing genetic potential and the inferred taxa harboring those genes by sequencing nifH gene fragments in samples taken along a permafrost thaw gradient in an Alaskan boreal soil. Samples from minimally, moderately and extensively thawed sites were taken to a depth of 79 cm to encompass zones above and below the depth of the water table. NifH reads were translated with frameshift correction and 112,476 sequences were clustered at 5% amino acid dissimilarity resulting in 1,631 OTUs. Sample depth in relation to water table depth was correlated to differences in the NifH sequence classes with those most closely related to group I nifH-harboring Alpha- and Beta-Proteobacteria in higher abundance above water table depth while those related to group III nifH-harboring Delta Proteobacteria more abundant below. The most dominant below water table depth NifH sequences, comprising 1/3 of the total, were distantly related to Verrucomicrobia-Opitutaceae. Overall, these results suggest that permafrost thaw alters the class-level composition of N2-fixing communities in the thawed soil layers and that this distinction corresponds to the depth of the water table. These nifH data were also compared to nifH sequences obtained from a study at an Alaskan taiga site, and to those of other geographically distant, non-permafrost sites. The two Alaska sites were differentiated largely by changes in relative abundances of the same OTUs, whereas the non-Alaska sites were differentiated by the lack of many Alaskan OTUs, and the presence of unique halophilic, sulfate- and iron-reducing taxa in the Alaska sites.},
doi = {10.3389/fmicb.2016.01894},
journal = {Frontiers in Microbiology},
number = NOV,
volume = 7,
place = {United States},
year = {Thu Nov 24 00:00:00 EST 2016},
month = {Thu Nov 24 00:00:00 EST 2016}
}

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Molecular Diversity of nifH Genes from Bacteria Associated with High Arctic Dwarf Shrubs
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journal, June 2008


Plant Species Composition and Productivity following Permafrost Thaw and Thermokarst in Alaskan Tundra
journal, March 2007


Soil biogeochemistry during the early spring in low arctic mesic tundra and the impacts of deepened snow and enhanced nitrogen availability
journal, December 2009


Bryophyte-cyanobacterial associations as a key factor in N2-fixation across the Canadian Arctic
journal, March 2011


How is nitrogen fixation in the high arctic linked to greenhouse gas emissions?
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Stream geochemistry as an indicator of increasing permafrost thaw depth in an arctic watershed
journal, April 2010


Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities
journal, February 2004


Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil
journal, January 2011


Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high arctic tundra soils
journal, June 2008

  • Walker, Jennifer K. M.; Egger, Keith N.; Henry, Gregory H. R.
  • The ISME Journal, Vol. 2, Issue 9
  • DOI: 10.1038/ismej.2008.52

Evidence for the functional significance of diazotroph community structure in soil
journal, September 2008


Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization
journal, September 2004

  • Mack, Michelle C.; Schuur, Edward A. G.; Bret-Harte, M. Syndonia
  • Nature, Vol. 431, Issue 7007
  • DOI: 10.1038/nature02887

The effect of permafrost thaw on old carbon release and net carbon exchange from tundra
journal, May 2009

  • Schuur, Edward A. G.; Vogel, Jason G.; Crummer, Kathryn G.
  • Nature, Vol. 459, Issue 7246
  • DOI: 10.1038/nature08031

Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw
journal, November 2011

  • Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M.
  • Nature, Vol. 480, Issue 7377
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Controls over carbon storage and turnover in high-latitude soils
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Nitrogenase gene diversity and microbial community structure: a cross-system comparison
journal, July 2003


From The Cover: Plant community responses to experimental warming across the tundra biome
journal, January 2006

  • Walker, M. D.; Wahren, C. H.; Hollister, R. D.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 5
  • DOI: 10.1073/pnas.0503198103

The Natural History of Nitrogen Fixation
journal, March 2004

  • Raymond, Jason; Siefert, Janet L.; Staples, Christopher R.
  • Molecular Biology and Evolution, Vol. 21, Issue 3
  • DOI: 10.1093/molbev/msh047

MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013

  • Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
  • Molecular Biology and Evolution, Vol. 30, Issue 12
  • DOI: 10.1093/molbev/mst197

Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011

  • Letunic, I.; Bork, P.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr201

Potential carbon release from permafrost soils of Northeastern Siberia
journal, December 2006


Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra: WARMING OF ALASKAN TUNDRA
journal, February 2011


A frozen feast: thawing permafrost increases plant-available nitrogen in subarctic peatlands
journal, March 2012


Seasonal and site-specific variations in nitrogen fixation in a high arctic area, Ny-Ålesund, Spitsbergen
journal, August 1997

  • Liengen, Turid; Olsen, Rolf Arnt
  • Canadian Journal of Microbiology, Vol. 43, Issue 8
  • DOI: 10.1139/m97-109

Changes in N-Transforming Archaea and Bacteria in Soil during the Establishment of Bioenergy Crops
journal, September 2011


A Comprehensive Evaluation of PCR Primers to Amplify the nifH Gene of Nitrogenase
journal, July 2012


The Nitrogen Balance of Arctic Tundra: Pathways, Rates, and Environmental Implications1
journal, January 1975


Dinitrogen Fixation (Acetylene Reduction) in High Arctic Sedge Meadow Communities
journal, May 1986

  • Henry, Greg H. R.; Svoboda, Josef
  • Arctic and Alpine Research, Vol. 18, Issue 2
  • DOI: 10.2307/1551127

Nitrogen Mineralization, Nitrification, and Denitrification in a High Arctic Lowland Ecosystem, Devon Island, N.W.T., Canada
journal, February 1996

  • Chapin, David M.
  • Arctic and Alpine Research, Vol. 28, Issue 1
  • DOI: 10.2307/1552089

Nitrification Potentials in Primary and Secondary Succession
journal, April 1981

  • Robertson, G. Philip; Vitousek, Peter M.
  • Ecology, Vol. 62, Issue 2
  • DOI: 10.2307/1936712

Biogeochemical Diversity Along a Riverside Toposequence in Arctic Alaska
journal, February 1991

  • Giblin, A. E.; Nadelhoffer, K. J.; Shaver, G. R.
  • Ecological Monographs, Vol. 61, Issue 4
  • DOI: 10.2307/2937049

Functional genes to assess nitrogen cycling and aromatic hydrocarbon degradation: primers and processing matter
journal, January 2013

  • Penton, C. Ryan; Johnson, Timothy A.; Quensen, John F.
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00279

Metagenomics Reveals Pervasive Bacterial Populations and Reduced Community Diversity across the Alaska Tundra Ecosystem
journal, April 2016

  • Johnston, Eric R.; Rodriguez-R, Luis M.; Luo, Chengwei
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00579

Works referencing / citing this record:

Microbial functional diversity covaries with permafrost thaw-induced environmental heterogeneity in tundra soil
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Diazotroph Diversity and Nitrogen Fixation in Summer Active Perennial Grasses in a Mediterranean Region Agricultural Soil
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