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Title: Biogeographic patterns of soil diazotrophic communities across six forests in the North America

Abstract

Soil diazotrophs play important roles in ecosystem functioning by converting atmospheric N2 into biologically available ammonium. However, the diversity and distribution of soil diazotrophic communities in different forests and whether they follow biogeographic patterns similar to macroorganisms still remain unclear. By sequencing nifH gene amplicons, we surveyed the diversity, structure and biogeographic patterns of soil diazotrophic communities across six North American forests (126 nested samples). Our results showed that each forest harboured markedly different soil diazotrophic communities and that these communities followed traditional biogeographic patterns similar to plant and animal communities, including the taxa–area relationship (TAR) and latitudinal diversity gradient. Significantly higher community diversity and lower microbial spatial turnover rates (i.e. z-values) were found for rainforests (~0.06) than temperate forests (~0.1). The gradient pattern of TARs and community diversity was strongly correlated (r2 > 0.5) with latitude, annual mean temperature, plant species richness and precipitation, and weakly correlated (r2 < 0.25) with pH and soil moisture. Here, this study suggests that even microbial subcommunities (e.g. soil diazotrophs) follow general biogeographic patterns (e.g. TAR, latitudinal diversity gradient), and indicates that the metabolic theory of ecology and habitat heterogeneity may be the major underlying ecological mechanisms shaping the biogeographic patterns of soilmore » diazotrophic communities.« less

Authors:
 [1];  [2];  [3];  [3];  [4];  [3];  [3];  [3];  [5];  [6];  [7]; ORCiD logo [8];  [9];  [10];  [10];  [11]
  1. Zhejiang Univ. of Technology, Zhejiang (China); Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
  2. Chinese Academy of Sciences (CAS), Beijing (China)
  3. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
  4. Zhejiang Univ. of Technology, Zhejiang (China)
  5. Univ. of Arizona, Tucson, AZ (United States)
  6. Univ. of Arizona, Tucson, AZ (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  7. Univ. of Arizona, Tucson, AZ (United States); Santa Fe Inst., Santa Fe, NM (United States)
  8. Univ. of Oklahoma, Norman, OK (United States)
  9. Univ. of Oklahoma, Norman, OK (United States); Smithsonian Tropical Research Inst., Balboa (Panama)
  10. Univ. of New Mexico, Albuquerque, NM (United States)
  11. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics; Tsinghua Univ., Beijing (China); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
National Science Foundation (NSF)
OSTI Identifier:
1581100
Grant/Contract Number:  
AC02-05CH11231; NSF EF-1065844
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Ecology
Additional Journal Information:
Journal Volume: 25; Journal Issue: 12; Journal ID: ISSN 0962-1083
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biogeography; diversity gradients; nifH; soil diazotrophs; taxa–area relationship

Citation Formats

Tu, Qichao, Deng, Ye, Yan, Qingyun, Shen, Lina, Lin, Lu, He, Zhili, Wu, Liyou, Van Nostrand, Joy D., Buzzard, Vanessa, Michaletz, Sean T., Enquist, Brian J., Weiser, Michael D., Kaspari, Michael, Waide, Robert B., Brown, James H., and Zhou, Jizhong. Biogeographic patterns of soil diazotrophic communities across six forests in the North America. United States: N. p., 2016. Web. doi:10.1111/mec.13651.
Tu, Qichao, Deng, Ye, Yan, Qingyun, Shen, Lina, Lin, Lu, He, Zhili, Wu, Liyou, Van Nostrand, Joy D., Buzzard, Vanessa, Michaletz, Sean T., Enquist, Brian J., Weiser, Michael D., Kaspari, Michael, Waide, Robert B., Brown, James H., & Zhou, Jizhong. Biogeographic patterns of soil diazotrophic communities across six forests in the North America. United States. https://doi.org/10.1111/mec.13651
Tu, Qichao, Deng, Ye, Yan, Qingyun, Shen, Lina, Lin, Lu, He, Zhili, Wu, Liyou, Van Nostrand, Joy D., Buzzard, Vanessa, Michaletz, Sean T., Enquist, Brian J., Weiser, Michael D., Kaspari, Michael, Waide, Robert B., Brown, James H., and Zhou, Jizhong. Sun . "Biogeographic patterns of soil diazotrophic communities across six forests in the North America". United States. https://doi.org/10.1111/mec.13651. https://www.osti.gov/servlets/purl/1581100.
@article{osti_1581100,
title = {Biogeographic patterns of soil diazotrophic communities across six forests in the North America},
author = {Tu, Qichao and Deng, Ye and Yan, Qingyun and Shen, Lina and Lin, Lu and He, Zhili and Wu, Liyou and Van Nostrand, Joy D. and Buzzard, Vanessa and Michaletz, Sean T. and Enquist, Brian J. and Weiser, Michael D. and Kaspari, Michael and Waide, Robert B. and Brown, James H. and Zhou, Jizhong},
abstractNote = {Soil diazotrophs play important roles in ecosystem functioning by converting atmospheric N2 into biologically available ammonium. However, the diversity and distribution of soil diazotrophic communities in different forests and whether they follow biogeographic patterns similar to macroorganisms still remain unclear. By sequencing nifH gene amplicons, we surveyed the diversity, structure and biogeographic patterns of soil diazotrophic communities across six North American forests (126 nested samples). Our results showed that each forest harboured markedly different soil diazotrophic communities and that these communities followed traditional biogeographic patterns similar to plant and animal communities, including the taxa–area relationship (TAR) and latitudinal diversity gradient. Significantly higher community diversity and lower microbial spatial turnover rates (i.e. z-values) were found for rainforests (~0.06) than temperate forests (~0.1). The gradient pattern of TARs and community diversity was strongly correlated (r2 > 0.5) with latitude, annual mean temperature, plant species richness and precipitation, and weakly correlated (r2 < 0.25) with pH and soil moisture. Here, this study suggests that even microbial subcommunities (e.g. soil diazotrophs) follow general biogeographic patterns (e.g. TAR, latitudinal diversity gradient), and indicates that the metabolic theory of ecology and habitat heterogeneity may be the major underlying ecological mechanisms shaping the biogeographic patterns of soil diazotrophic communities.},
doi = {10.1111/mec.13651},
journal = {Molecular Ecology},
number = 12,
volume = 25,
place = {United States},
year = {Sun Apr 17 00:00:00 EDT 2016},
month = {Sun Apr 17 00:00:00 EDT 2016}
}

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Works referenced in this record:

Over 150 Years of Long-Term Fertilization Alters Spatial Scaling of Microbial Biodiversity
journal, April 2015


Application of a nifH oligonucleotide microarray for profiling diversity of N 2 -fixing microorganisms in marine microbial mats
journal, October 2006


The Canonical Distribution of Commonness and Rarity: Part I
journal, April 1962


Microbial biogeography: putting microorganisms on the map
journal, February 2006

  • Martiny, Jennifer B. Hughes; Bohannan, Brendan J. M.; Brown, James H.
  • Nature Reviews Microbiology, Vol. 4, Issue 2
  • DOI: 10.1038/nrmicro1341

Global patterns in biodiversity
journal, May 2000


Comparison of nifH Gene Pools in Soils and Soil Microenvironments with Contrasting Properties
journal, May 2001


Global Dispersal of Free-Living Microbial Eukaryote Species
journal, May 2002


Nutrient-cycling microbes in coastal Douglas-fir forests: regional-scale correlation between communities, in situ climate, and other factors
journal, October 2015

  • Shay, Philip-Edouard; Winder, Richard S.; Trofymow, J. A.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01097

Nitrogen Fertilization Has a Stronger Effect on Soil Nitrogen-Fixing Bacterial Communities than Elevated Atmospheric CO 2
journal, March 2014

  • Berthrong, Sean T.; Yeager, Chris M.; Gallegos-Graves, Laverne
  • Applied and Environmental Microbiology, Vol. 80, Issue 10
  • DOI: 10.1128/AEM.04034-13

The Ubiquity of Small Species: Patterns of Local and Global Diversity
journal, January 2004


Reproducibility and quantitation of amplicon sequencing-based detection
journal, February 2011


Global marine bacterial diversity peaks at high latitudes in winter
journal, March 2013

  • Ladau, Joshua; Sharpton, Thomas J.; Finucane, Mariel M.
  • The ISME Journal, Vol. 7, Issue 9
  • DOI: 10.1038/ismej.2013.37

Global patterns of diversity and community structure in marine bacterioplankton: MARINE BACTERIA DIVERSITY and DISTRIBUTION
journal, December 2006


Emergent Biogeography of Microbial Communities in a Model Ocean
journal, March 2007


Loss in microbial diversity affects nitrogen cycling in soil
journal, March 2013

  • Philippot, Laurent; Spor, Aymé; Hénault, Catherine
  • The ISME Journal, Vol. 7, Issue 8
  • DOI: 10.1038/ismej.2013.34

Nitrogen limitation on land and in the sea: How can it occur?
journal, January 1991

  • Vitousek, PeterM.; Howarth, RobertW.
  • Biogeochemistry, Vol. 13, Issue 2
  • DOI: 10.1007/BF00002772

Randomness, Area, and Species Richness
journal, August 1982

  • Coleman, Bernard D.; Mares, Michael A.; Willig, Michael R.
  • Ecology, Vol. 63, Issue 4
  • DOI: 10.2307/1937249

Abundances and Distributions of the Dominant nifH Phylotypes in the Northern Atlantic Ocean
journal, February 2008

  • Langlois, R. J.; Hummer, D.; LaRoche, J.
  • Applied and Environmental Microbiology, Vol. 74, Issue 6
  • DOI: 10.1128/AEM.01720-07

FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Nitrogen Cycles: Past, Present, and Future
journal, September 2004


Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography
journal, April 2007


Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis
journal, June 2015


Latitudinal Gradients of Biodiversity: Pattern, Process, Scale, and Synthesis
journal, November 2003


On random placement and species-area relations
journal, June 1981


MEGAN analysis of metagenomic data
journal, February 2007

  • Huson, D. H.; Auch, A. F.; Qi, J.
  • Genome Research, Vol. 17, Issue 3
  • DOI: 10.1101/gr.5969107

Are There General Laws in Ecology?
journal, February 1999


PicoGreen quantitation of DNA: effective evaluation of samples pre- or post-PCR
journal, July 1996


UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013


Habitat heterogeneity overrides the species–area relationship
journal, April 2008


Toward a Metabolic Theory of Ecology
journal, July 2004

  • Brown, James H.; Gillooly, James F.; Allen, Andrew P.
  • Ecology, Vol. 85, Issue 7
  • DOI: 10.1890/03-9000

Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants
journal, December 2008

  • Franche, Claudine; Lindström, Kristina; Elmerich, Claudine
  • Plant and Soil, Vol. 321, Issue 1-2
  • DOI: 10.1007/s11104-008-9833-8

Plant Species Diversity in Old-Field Successional Ecosystems in Southern Illinois
journal, March 1975


Distribution of Extensive nifH Gene Diversity Across Physical Soil Microenvironments
journal, April 2006


Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants
journal, July 2007


Time and Space and the Variation of Species
journal, October 1960


Global diversity and geography of soil fungi
journal, November 2014


Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients
journal, December 2011

  • Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S.
  • The ISME Journal, Vol. 6, Issue 5
  • DOI: 10.1038/ismej.2011.159

Global patterns of terrestrial biological nitrogen (N 2 ) fixation in natural ecosystems
journal, June 1999

  • Cleveland, Cory C.; Townsend, Alan R.; Schimel, David S.
  • Global Biogeochemical Cycles, Vol. 13, Issue 2
  • DOI: 10.1029/1999GB900014

Pole-to-pole biogeography of surface and deep marine bacterial communities
journal, October 2012

  • Ghiglione, J. -F.; Galand, P. E.; Pommier, T.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 43
  • DOI: 10.1073/pnas.1208160109

The bacterial biogeography of British soils: Mapping soil bacteria
journal, April 2011


The Statistics and Biology of the Species-Area Relationship
journal, June 1979

  • Connor, Edward F.; McCoy, Earl D.
  • The American Naturalist, Vol. 113, Issue 6
  • DOI: 10.1086/283438

A taxa–area relationship for bacteria
journal, December 2004

  • Horner-Devine, M. Claire; Lage, Melissa; Hughes, Jennifer B.
  • Nature, Vol. 432, Issue 7018
  • DOI: 10.1038/nature03073

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Spatial scaling of microbial eukaryote diversity
journal, December 2004

  • Green, Jessica L.; Holmes, Andrew J.; Westoby, Mark
  • Nature, Vol. 432, Issue 7018
  • DOI: 10.1038/nature03034

Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes: Bacterial biogeography in arctic soils
journal, November 2010


Doubling of marine dinitrogen-fixation rates based on direct measurements
journal, August 2012

  • Großkopf, Tobias; Mohr, Wiebke; Baustian, Tina
  • Nature, Vol. 488, Issue 7411
  • DOI: 10.1038/nature11338

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


Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges
journal, November 2008


Nitrogenase gene diversity and microbial community structure: a cross-system comparison
journal, July 2003


Species–area relationships explained by the joint effects of dispersal limitation and habitat heterogeneity
journal, November 2009

  • Shen, Guochun; Yu, Mingjian; Hu, Xin-Sheng
  • Ecology, Vol. 90, Issue 11
  • DOI: 10.1890/08-1646.1

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

A strong species?area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi
journal, June 2007


Genomic insights that advance the species definition for prokaryotes
journal, February 2005

  • Konstantinidis, K. T.; Tiedje, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
  • DOI: 10.1073/pnas.0409727102

Spatial scaling of functional gene diversity across various microbial taxa
journal, May 2008

  • Zhou, J.; Kang, S.; Schadt, C. W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 22
  • DOI: 10.1073/pnas.0709016105

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Spatial scaling of microbial biodiversity
journal, September 2006


Nitrogen fixation by marine cyanobacteria
journal, April 2011


On the Generality of the Latitudinal Diversity Gradient
journal, February 2004

  • Hillebrand, Helmut
  • The American Naturalist, Vol. 163, Issue 2
  • DOI: 10.1086/381004

Microbial community structure and its functional implications
journal, May 2009


A latitudinal diversity gradient in planktonic marine bacteria
journal, May 2008

  • Fuhrman, J. A.; Steele, J. A.; Hewson, I.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 22
  • DOI: 10.1073/pnas.0803070105

The Diversity and Co-occurrence Patterns of N2-Fixing Communities in a CO2-Enriched Grassland Ecosystem
journal, August 2015


nifH pyrosequencing reveals the potential for location-specific soil chemistry to influence N 2 -fixing community dynamics : N
journal, March 2014

  • Collavino, Mónica M.; Tripp, H. James; Frank, Ildiko E.
  • Environmental Microbiology, Vol. 16, Issue 10
  • DOI: 10.1111/1462-2920.12423

Works referencing / citing this record:

Differentiations of determinants for the community compositions of bacteria, fungi, and nitrogen fixers in various steppes
journal, February 2019

  • Sheng, Rong; Li, Ke; Zhang, Wenzhao
  • Ecology and Evolution, Vol. 9, Issue 6
  • DOI: 10.1002/ece3.4940

Soil microbiotic homogenization occurred after long‐term agricultural development in desert areas across northern China
journal, January 2020

  • Liu, Jie; Xu, Aiai; Wang, Changkun
  • Land Degradation & Development, Vol. 31, Issue 8
  • DOI: 10.1002/ldr.3521

Soil parameters, land use, and geographical distance drive soil bacterial communities along a European transect
journal, January 2019

  • Plassart, Pierre; Prévost-Bouré, Nicolas Chemidlin; Uroz, Stéphane
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-018-36867-2

NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes
journal, August 2018


Spatial scaling of forest soil microbial communities across a temperature gradient: Temperature altered microbial spatial scaling
journal, September 2018


Analysis of nifH DNA and RNA reveals a disproportionate contribution to nitrogenase activities by rare plankton-associated diazotrophs
journal, August 2019


Plant functional traits determine latitudinal variations in soil microbial function: evidence from forests in China
journal, January 2019


Differentiations of determinants for the community compositions of bacteria, fungi, and nitrogen fixers in various steppes
journal, February 2019

  • Sheng, Rong; Li, Ke; Zhang, Wenzhao
  • Ecology and Evolution, Vol. 9, Issue 6
  • DOI: 10.1002/ece3.4940

Soil parameters, land use, and geographical distance drive soil bacterial communities along a European transect
journal, January 2019

  • Plassart, Pierre; Prévost-Bouré, Nicolas Chemidlin; Uroz, Stéphane
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-018-36867-2