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Title: The spatial scale dependence of diazotrophic and bacterial community assembly in paddy soil

Abstract

Aim: The factors driving microbial community β-diversity (variation in composition) at different spatial scales yield fundamental insights into the mechanisms that maintain ecosystem biodiversity, which as yet are uncertain. In this work, we explore whether spatial scale-dependent patterns of β-diversity vary between microbial functional groups and bacterial taxa (i.e., diazotrophic and bacterial communities) across local to regional scales (from metres to hundreds of kilometres). Location: Eastern China. Time period: October and November 2015. Major taxa studied: Diazotrophic and bacterial communities. Methods: We use two complementary statistical tools to unveil biotic mechanisms (i.e., species association) underlying variation in β-diversity of diazotrophic and bacterial communities. We examined distance–decay slopes of both communities at the local (1–113 m), meso- (3.4–39 km) and regional (103–668 km) scales. We used an environmentally constrained checkerboard score and topological features of association networks as indices of species association. We then calculated contributions of species association, abiotic factors and geographical distance to explain community β-diversity. The scale-dependent distance–decay relationships were also examined in ubiquitous (high occupancy across samples) and endemic communities of diazotrophs and bacteria. Results: Diazotrophs displayed steeper distance–decay slopes than bacteria, suggesting that the β-diversity of diazotrophic communities was more variable. The distance–decay slopes were dependent on spatial scalesmore » in both communities, owing to different contributions of geographical distance, abiotic factors and species association at three spatial scales. Intriguingly, species association was greater and contributed more to community β-diversity than other forces at the local scale, implying that species association could greatly alter community structures. Main conclusions: Drivers of diazotrophic and bacterial community β-diversity depended on spatial scales, resulting in different distance–decay patterns. Moreover, this was the first study to use two methods to demonstrate that species association played important, but as yet unrecognized, roles in driving spatial scale-dependent β-diversity.« less

Authors:
ORCiD logo [1];  [1];  [2];  [2];  [1];  [2];  [3];  [1];  [1];  [4];  [1];  [1];  [4];  [4];  [1];  [5];  [5];  [5];  [6];  [7]
  1. Tsinghua Univ., Beijing (China). School of Environment, State Key Joint Laboratory of Environment Simulation and Pollution Control
  2. Univ. of Oklahoma, Norman, OK (United States). Dept. of Microbiology and Plant Biology, Inst. for Environmental Genomics
  3. Univ. of Oklahoma, Norman, OK (United States). Dept. of Microbiology and Plant Biology, Inst. for Environmental Genomics; US Dept. of Agriculture (USDA), Parlier, CA (United States). Agricultural Research Service, San Joaquin Valley Agricultural Sciences Center
  4. Department of Microbiology and Plant Biology, Institute for Environmental Genomics University of Oklahoma Norman Oklahoma
  5. Chinese Academy of Sciences (CAS), Nanjing (China). State Key Laboratory of Soil and Sustainable Agriculture, Inst. of Soil Science
  6. Tsinghua Univ., Beijing (China). School of Environment, State Key Joint Laboratory of Environment Simulation and Pollution Control; Univ. of Oklahoma, Norman, OK (United States). Dept. of Microbiology and Plant Biology, Inst. for Environmental Genomics; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences
  7. Univ. of Helsinki (Finland)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Chinese Academy of Sciences; State Key Joint Laboratory of Environment Simulation and Pollution Control (China); National Natural Science Foundation of China (NNSFC)
OSTI Identifier:
1580844
Grant/Contract Number:  
AC02-05CH11231; XDB15010102; 17L03ESPC; 41430856; 41825016
Resource Type:
Accepted Manuscript
Journal Name:
Global Ecology and Biogeography
Additional Journal Information:
Journal Volume: 28; Journal Issue: 8; Journal ID: ISSN 1466-822X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; 60 APPLIED LIFE SCIENCES; bacterial community; β‐diversity; community assembly; diazotrophic community; paddy soil; spatial scale dependence; species association

Citation Formats

Gao, Qun, Yang, Yunfeng, Feng, Jiajie, Tian, Renmao, Guo, Xue, Ning, Daliang, Hale, Lauren, Wang, Mengmeng, Cheng, Jingmin, Wu, Linwei, Zhao, Mengxin, Zhao, Jianshu, Wu, Liyou, Qin, Yujia, Qi, Qi, Liang, Yuting, Sun, Bo, Chu, Haiyan, Zhou, Jizhong, and Soininen, Janne. The spatial scale dependence of diazotrophic and bacterial community assembly in paddy soil. United States: N. p., 2019. Web. doi:10.1111/geb.12917.
Gao, Qun, Yang, Yunfeng, Feng, Jiajie, Tian, Renmao, Guo, Xue, Ning, Daliang, Hale, Lauren, Wang, Mengmeng, Cheng, Jingmin, Wu, Linwei, Zhao, Mengxin, Zhao, Jianshu, Wu, Liyou, Qin, Yujia, Qi, Qi, Liang, Yuting, Sun, Bo, Chu, Haiyan, Zhou, Jizhong, & Soininen, Janne. The spatial scale dependence of diazotrophic and bacterial community assembly in paddy soil. United States. doi:10.1111/geb.12917.
Gao, Qun, Yang, Yunfeng, Feng, Jiajie, Tian, Renmao, Guo, Xue, Ning, Daliang, Hale, Lauren, Wang, Mengmeng, Cheng, Jingmin, Wu, Linwei, Zhao, Mengxin, Zhao, Jianshu, Wu, Liyou, Qin, Yujia, Qi, Qi, Liang, Yuting, Sun, Bo, Chu, Haiyan, Zhou, Jizhong, and Soininen, Janne. Mon . "The spatial scale dependence of diazotrophic and bacterial community assembly in paddy soil". United States. doi:10.1111/geb.12917.
@article{osti_1580844,
title = {The spatial scale dependence of diazotrophic and bacterial community assembly in paddy soil},
author = {Gao, Qun and Yang, Yunfeng and Feng, Jiajie and Tian, Renmao and Guo, Xue and Ning, Daliang and Hale, Lauren and Wang, Mengmeng and Cheng, Jingmin and Wu, Linwei and Zhao, Mengxin and Zhao, Jianshu and Wu, Liyou and Qin, Yujia and Qi, Qi and Liang, Yuting and Sun, Bo and Chu, Haiyan and Zhou, Jizhong and Soininen, Janne},
abstractNote = {Aim: The factors driving microbial community β-diversity (variation in composition) at different spatial scales yield fundamental insights into the mechanisms that maintain ecosystem biodiversity, which as yet are uncertain. In this work, we explore whether spatial scale-dependent patterns of β-diversity vary between microbial functional groups and bacterial taxa (i.e., diazotrophic and bacterial communities) across local to regional scales (from metres to hundreds of kilometres). Location: Eastern China. Time period: October and November 2015. Major taxa studied: Diazotrophic and bacterial communities. Methods: We use two complementary statistical tools to unveil biotic mechanisms (i.e., species association) underlying variation in β-diversity of diazotrophic and bacterial communities. We examined distance–decay slopes of both communities at the local (1–113 m), meso- (3.4–39 km) and regional (103–668 km) scales. We used an environmentally constrained checkerboard score and topological features of association networks as indices of species association. We then calculated contributions of species association, abiotic factors and geographical distance to explain community β-diversity. The scale-dependent distance–decay relationships were also examined in ubiquitous (high occupancy across samples) and endemic communities of diazotrophs and bacteria. Results: Diazotrophs displayed steeper distance–decay slopes than bacteria, suggesting that the β-diversity of diazotrophic communities was more variable. The distance–decay slopes were dependent on spatial scales in both communities, owing to different contributions of geographical distance, abiotic factors and species association at three spatial scales. Intriguingly, species association was greater and contributed more to community β-diversity than other forces at the local scale, implying that species association could greatly alter community structures. Main conclusions: Drivers of diazotrophic and bacterial community β-diversity depended on spatial scales, resulting in different distance–decay patterns. Moreover, this was the first study to use two methods to demonstrate that species association played important, but as yet unrecognized, roles in driving spatial scale-dependent β-diversity.},
doi = {10.1111/geb.12917},
journal = {Global Ecology and Biogeography},
number = 8,
volume = 28,
place = {United States},
year = {2019},
month = {5}
}

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Works referenced in this record:

The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update
journal, May 2016

  • Afgan, Enis; Baker, Dannon; van den Beek, Marius
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw343

Decoupled distance-decay patterns between dsrA and 16S rRNA genes among salt marsh sulfate-reducing bacteria: Biogeography of sulfate-reducing bacteria
journal, April 2015

  • Angermeyer, Angus; Crosby, Sarah C.; Huber, Julie A.
  • Environmental Microbiology, Vol. 18, Issue 1
  • DOI: 10.1111/1462-2920.12821

Euxinic Freshwater Hypolimnia Promote Bacterial Endemicity in Continental Areas
journal, November 2010


Using network analysis to explore co-occurrence patterns in soil microbial communities
journal, September 2011

  • Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O.
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.119

Experimental tests of the bacterial distance–decay relationship
journal, June 2010


Deciphering microbial interactions and detecting keystone species with co-occurrence networks
journal, May 2014


Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development
journal, August 2015

  • Burns, Adam R.; Stephens, W. Zac; Stagaman, Keaton
  • The ISME Journal, Vol. 10, Issue 3
  • DOI: 10.1038/ismej.2015.142

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

A theory for species co-occurrence in interaction networks
journal, October 2015


A global network of coexisting microbes from environmental and whole-genome sequence data
journal, May 2010

  • Chaffron, S.; Rehrauer, H.; Pernthaler, J.
  • Genome Research, Vol. 20, Issue 7
  • DOI: 10.1101/gr.104521.109

The Roles of Harsh and Fluctuating Conditions in the Dynamics of Ecological Communities
journal, November 1997

  • Chesson, Peter; Huntly, Nancy
  • The American Naturalist, Vol. 150, Issue 5
  • DOI: 10.1086/286080

Finding community structure in very large networks
journal, December 2004


Molecular ecological network analyses
journal, January 2012


ecospat: an R package to support spatial analyses and modeling of species niches and distributions
journal, February 2017

  • Di Cola, Valeria; Broennimann, Olivier; Petitpierre, Blaise
  • Ecography, Vol. 40, Issue 6
  • DOI: 10.1111/ecog.02671

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


UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems
journal, December 2007


Microbial interactions: from networks to models
journal, July 2012

  • Faust, Karoline; Raes, Jeroen
  • Nature Reviews Microbiology, Vol. 10, Issue 8
  • DOI: 10.1038/nrmicro2832

Embracing the unknown: disentangling the complexities of the soil microbiome
journal, August 2017


The large-scale organization of the bacterial network of ecological co-occurrence interactions
journal, February 2010

  • Freilich, Shiri; Kreimer, Anat; Meilijson, Isacc
  • Nucleic Acids Research, Vol. 38, Issue 12
  • DOI: 10.1093/nar/gkq118

Microbial community structure and its functional implications
journal, May 2009


Abiotic stress tolerance and competition-related traits underlie phylogenetic clustering in soil bacterial communities
journal, August 2014

  • Goberna, Marta; Navarro-Cano, Jose A.; Valiente-Banuet, Alfonso
  • Ecology Letters, Vol. 17, Issue 10
  • DOI: 10.1111/ele.12341

The ecodist Package for Dissimilarity-based Analysis of Ecological Data
journal, January 2007

  • Goslee, Sarah C.; Urban, Dean L.
  • Journal of Statistical Software, Vol. 22, Issue 7
  • DOI: 10.18637/jss.v022.i07

Spatial scaling of microbial biodiversity
journal, September 2006


Self-Similarity in the Distribution and Abundance of Species
journal, April 1999


Temporal and spatial scales of variation in bacterioplankton assemblages of oligotrophic surface waters
journal, April 2006

  • Hewson, I.; Steele, Ja; Capone, Dg
  • Marine Ecology Progress Series, Vol. 311
  • DOI: 10.3354/meps311067

Trade-offs in community ecology: linking spatial scales and species coexistence
journal, January 2004


Similarity and local co-existence of species in regional biotas
journal, January 1998


Long-term shifts in the patterns and underlying processes of plant associations in Wisconsin forests: Plant co-occurrence dynamics in Wisconsin
journal, January 2016

  • Li, Daijiang; Waller, Donald
  • Global Ecology and Biogeography, Vol. 25, Issue 5
  • DOI: 10.1111/geb.12432

Homogenization of species composition and species association networks are decoupled: XXXX
journal, October 2018

  • Li, Daijiang; Poisot, Timothée; Waller, Donald M.
  • Global Ecology and Biogeography, Vol. 27, Issue 12
  • DOI: 10.1111/geb.12825

Diversity and distribution patterns of acidobacterial communities in the black soil zone of northeast China
journal, April 2016


Efficient algorithms for accurate hierarchical clustering of huge datasets: tackling the entire protein space
journal, June 2008


Global patterns in bacterial diversity
journal, June 2007

  • Lozupone, C. A.; Knight, R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 27
  • DOI: 10.1073/pnas.0611525104

Application of random matrix theory to microarray data for discovering functional gene modules
journal, March 2006


Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China
journal, January 2016


The Limiting Similarity, Convergence, and Divergence of Coexisting Species
journal, September 1967

  • Macarthur, Robert; Levins, Richard
  • The American Naturalist, Vol. 101, Issue 921
  • DOI: 10.1086/282505

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

Drivers of bacterial  -diversity depend on spatial scale
journal, April 2011

  • Martiny, J. B. H.; Eisen, J. A.; Penn, K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 19
  • DOI: 10.1073/pnas.1016308108

Why do microbes exhibit weak biogeographic patterns?
journal, April 2018


A general framework for the distance-decay of similarity in ecological communities
journal, September 2008


The distance decay of similarity in biogeography and ecology
journal, July 1999


The Structure and Function of Complex Networks
journal, January 2003


Spatial scale drives patterns in soil bacterial diversity: Spatial scale drives soil diversity
journal, March 2016

  • O'Brien, Sarah L.; Gibbons, Sean M.; Owens, Sarah M.
  • Environmental Microbiology, Vol. 18, Issue 6
  • DOI: 10.1111/1462-2920.13231

Mapping the imprint of biotic interactions on β-diversity
journal, August 2018

  • Ohlmann, Marc; Mazel, Florent; Chalmandrier, Loïc
  • Ecology Letters, Vol. 21, Issue 11
  • DOI: 10.1111/ele.13143

NifH-Harboring Bacterial Community Composition across an Alaskan Permafrost Thaw Gradient
journal, November 2016


Ecological niche conservatism: a time-structured review of evidence: Ecological niche conservatism
journal, March 2011


The dissimilarity of species interaction networks
journal, September 2012

  • Poisot, Timothée; Canard, Elsa; Mouillot, David
  • Ecology Letters, Vol. 15, Issue 12
  • DOI: 10.1111/ele.12002

Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil
journal, January 2001


Network thinking in ecology and evolution
journal, June 2005


Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity
journal, February 2013

  • Ranjard, L.; Dequiedt, S.; Chemidlin Prévost-Bouré, N.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2431

The activated sludge ecosystem contains a core community of abundant organisms
journal, August 2015

  • Saunders, Aaron M.; Albertsen, Mads; Vollertsen, Jes
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.117

Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean
journal, October 2009

  • Schauer, Regina; Bienhold, Christina; Ramette, Alban
  • The ISME Journal, Vol. 4, Issue 2
  • DOI: 10.1038/ismej.2009.106

Dramatic Increases of Soil Microbial Functional Gene Diversity at the Treeline Ecotone of Changbai Mountain
journal, July 2016


The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages
journal, June 2016

  • Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J.
  • Ecology Letters, Vol. 19, Issue 8
  • DOI: 10.1111/ele.12630

Causes, consequences and ethics of biodiversity
journal, May 2000


Phylogenetic limiting similarity and competitive exclusion: Phylogenetic relatedness and competition
journal, June 2011


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

Taxa-area relationships for microbes: the unsampled and the unseen
journal, July 2006


Long-term successional dynamics of microbial association networks in anaerobic digestion processes
journal, November 2016


Phylogenetic imprint of woody plants on the soil mycobiome in natural mountain forests of eastern China
journal, October 2018


Metabolic dependencies drive species co-occurrence in diverse microbial communities
journal, May 2015

  • Zelezniak, Aleksej; Andrejev, Sergej; Ponomarova, Olga
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
  • DOI: 10.1073/pnas.1421834112

454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants
journal, December 2011


Soil bacterial endemism and potential functional redundancy in natural broadleaf forest along a latitudinal gradient
journal, June 2016

  • Zhang, Yuguang; Cong, Jing; Lu, Hui
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep28819

Functional Molecular Ecological Networks
journal, October 2010


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

Bacterial taxa-area and distance-decay relationships in marine environments
journal, January 2014

  • Zinger, L.; Boetius, A.; Ramette, A.
  • Molecular Ecology, Vol. 23, Issue 4
  • DOI: 10.1111/mec.12640