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Title: Conservation of Species- and Trait-Based Modeling Network Interactions in Extremely Acidic Microbial Community Assembly

Abstract

Understanding microbial interactions is essential to decipher the mechanisms of community assembly and their effects on ecosystem functioning, however, the conservation of species- and trait-based network interactions along environmental gradient remains largely unknown. Here, by using the network-based analyses with three paralleled data sets derived from 16S rRNA gene pyrosequencing, functional microarray, and predicted metagenome, we test our hypothesis that the network interactions of traits are more conserved than those of taxonomic measures, with significantly lower variation of network characteristics along the environmental gradient in acid mine drainage. The results showed that although the overall network characteristics remained similar, the structural variation was significantly lower at trait levels. The higher conserved individual node topological properties at trait level rather than at species level indicated that the responses of diverse traits remained relatively consistent even though different species played key roles under different environmental conditions. Additionally, the randomization tests revealed that it could not reject the null hypothesis that species-based correlations were random, while the tests suggested that correlation patterns of traits were non-random. Furthermore, relationships between trait-based network characteristics and environmental properties implied that trait-based networks might be more useful in reflecting the variation of ecosystem function. Taken together, ourmore » results suggest that deterministic trait-based community assembly results in greater conservation of network interaction, which may ensure ecosystem function across environmental regimes, emphasizing the potential importance of measuring the complexity and conservation of network interaction in evaluating the ecosystem stability and functioning.« less

Authors:
 [1];  [2];  [3];  [3];  [3];  [3];  [3];  [3];  [4];  [3]
  1. Sun Yat-Sen Univ., Guangzhou (China); Univ. of Oklahoma, Norman, OK (United States)
  2. Sun Yat-Sen Univ., Guangzhou (China); Univ. of Toronto-Scarborough, ON (Canada); Univ. of Toronto, ON (Canada)
  3. Sun Yat-Sen Univ., Guangzhou (China)
  4. 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); National Natural Science Foundation of China (NSFC)
OSTI Identifier:
1567095
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal Issue: AUG; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; community assembly; interacting relationship; network conservation; acid mine drainage

Citation Formats

Kuang, Jialiang, Cadotte, Marc W., Chen, Yongjian, Shu, Haoyue, Liu, Jun, Chen, Linxing, Hua, Zhengshuang, Shu, Wensheng, Zhou, Jizhong, and Huang, Linan. Conservation of Species- and Trait-Based Modeling Network Interactions in Extremely Acidic Microbial Community Assembly. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01486.
Kuang, Jialiang, Cadotte, Marc W., Chen, Yongjian, Shu, Haoyue, Liu, Jun, Chen, Linxing, Hua, Zhengshuang, Shu, Wensheng, Zhou, Jizhong, & Huang, Linan. Conservation of Species- and Trait-Based Modeling Network Interactions in Extremely Acidic Microbial Community Assembly. United States. https://doi.org/10.3389/fmicb.2017.01486
Kuang, Jialiang, Cadotte, Marc W., Chen, Yongjian, Shu, Haoyue, Liu, Jun, Chen, Linxing, Hua, Zhengshuang, Shu, Wensheng, Zhou, Jizhong, and Huang, Linan. Thu . "Conservation of Species- and Trait-Based Modeling Network Interactions in Extremely Acidic Microbial Community Assembly". United States. https://doi.org/10.3389/fmicb.2017.01486. https://www.osti.gov/servlets/purl/1567095.
@article{osti_1567095,
title = {Conservation of Species- and Trait-Based Modeling Network Interactions in Extremely Acidic Microbial Community Assembly},
author = {Kuang, Jialiang and Cadotte, Marc W. and Chen, Yongjian and Shu, Haoyue and Liu, Jun and Chen, Linxing and Hua, Zhengshuang and Shu, Wensheng and Zhou, Jizhong and Huang, Linan},
abstractNote = {Understanding microbial interactions is essential to decipher the mechanisms of community assembly and their effects on ecosystem functioning, however, the conservation of species- and trait-based network interactions along environmental gradient remains largely unknown. Here, by using the network-based analyses with three paralleled data sets derived from 16S rRNA gene pyrosequencing, functional microarray, and predicted metagenome, we test our hypothesis that the network interactions of traits are more conserved than those of taxonomic measures, with significantly lower variation of network characteristics along the environmental gradient in acid mine drainage. The results showed that although the overall network characteristics remained similar, the structural variation was significantly lower at trait levels. The higher conserved individual node topological properties at trait level rather than at species level indicated that the responses of diverse traits remained relatively consistent even though different species played key roles under different environmental conditions. Additionally, the randomization tests revealed that it could not reject the null hypothesis that species-based correlations were random, while the tests suggested that correlation patterns of traits were non-random. Furthermore, relationships between trait-based network characteristics and environmental properties implied that trait-based networks might be more useful in reflecting the variation of ecosystem function. Taken together, our results suggest that deterministic trait-based community assembly results in greater conservation of network interaction, which may ensure ecosystem function across environmental regimes, emphasizing the potential importance of measuring the complexity and conservation of network interaction in evaluating the ecosystem stability and functioning.},
doi = {10.3389/fmicb.2017.01486},
journal = {Frontiers in Microbiology},
number = AUG,
volume = 8,
place = {United States},
year = {Thu Aug 10 00:00:00 EDT 2017},
month = {Thu Aug 10 00:00:00 EDT 2017}
}

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Works referenced in this record:

Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria
journal, April 2014

  • Barberán, Albert; Ramirez, Kelly S.; Leff, Jonathan W.
  • Ecology Letters, Vol. 17, Issue 7
  • DOI: 10.1111/ele.12282

The ecology of differences: assessing community assembly with trait and evolutionary distances
journal, August 2013

  • Cadotte, Marc; Albert, Cecile H.; Walker, Steve C.
  • Ecology Letters, Vol. 16, Issue 10
  • DOI: 10.1111/ele.12161

Microbial interactions: from networks to models
journal, July 2012

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

Toward molecular trait‐based ecology through integration of biogeochemical, geographical and metagenomic data
journal, January 2011

  • Raes, Jeroen; Letunic, Ivica; Yamada, Takuji
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.6

AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature
journal, February 2010

  • Denef, Vincent J.; Mueller, Ryan S.; Banfield, Jillian F.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.158

Community structure of marine bacterioplankton: patterns, networks, and relationships to function
journal, September 2008

  • Fuhrman, Ja; Steele, Ja
  • Aquatic Microbial Ecology, Vol. 53
  • DOI: 10.3354/ame01222

Contemporary environmental variation determines microbial diversity patterns in acid mine drainage
journal, November 2012

  • Kuang, Jia-Liang; Huang, Li-Nan; Chen, Lin-Xing
  • The ISME Journal, Vol. 7, Issue 5
  • DOI: 10.1038/ismej.2012.139

Historical Contingency in Community Assembly: Integrating Niches, Species Pools, and Priority Effects
journal, December 2015


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

Species divergence and trait convergence in experimental plant community assembly
journal, December 2005


Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013

  • Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
  • Nature Biotechnology, Vol. 31, Issue 9
  • DOI: 10.1038/nbt.2676

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27

Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2
journal, July 2011


Rebuilding community ecology from functional traits
journal, April 2006


Molecular eco-systems biology: towards an understanding of community function
journal, June 2008

  • Raes, Jeroen; Bork, Peer
  • Nature Reviews Microbiology, Vol. 6, Issue 9
  • DOI: 10.1038/nrmicro1935

Correlation detection strategies in microbial data sets vary widely in sensitivity and precision
journal, February 2016

  • Weiss, Sophie; Van Treuren, Will; Lozupone, Catherine
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.235

Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory
journal, January 2007


Inferring Correlation Networks from Genomic Survey Data
journal, September 2012


Phylogenetic diversity promotes ecosystem stability
journal, August 2012

  • Cadotte, Marc W.; Dinnage, Russell; Tilman, David
  • Ecology, Vol. 93, Issue sp8
  • DOI: 10.1890/11-0426.1

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


Artefacts in statistical analyses of network motifs: general framework and application to metabolic networks
journal, July 2012

  • Beber, Moritz Emanuel; Fretter, Christoph; Jain, Shubham
  • Journal of The Royal Society Interface, Vol. 9, Issue 77
  • DOI: 10.1098/rsif.2012.0490

Microbial Biogeography: From Taxonomy to Traits
journal, May 2008


Finding community structure in very large networks
journal, December 2004


Marine bacterial, archaeal and protistan association networks reveal ecological linkages
journal, March 2011

  • Steele, Joshua A.; Countway, Peter D.; Xia, Li
  • The ISME Journal, Vol. 5, Issue 9
  • DOI: 10.1038/ismej.2011.24

Molecular ecological network analyses
journal, January 2012


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

Phylogenetic analysis of community assembly and structure over space and time
journal, November 2008


Specificity and Stability in Topology of Protein Networks
journal, May 2002


Structure and function of the global ocean microbiome
journal, May 2015


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

An index of ecosystem diversity
journal, December 1991


Inferring Cellular Networks Using Probabilistic Graphical Models
journal, February 2004


Bacterial community assembly based on functional genes rather than species
journal, August 2011

  • Burke, C.; Steinberg, P.; Rusch, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
  • DOI: 10.1073/pnas.1101591108

Microbial community transcriptional networks are conserved in three domains at ocean basin scales
journal, March 2015

  • Aylward, Frank O.; Eppley, John M.; Smith, Jason M.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 17
  • DOI: 10.1073/pnas.1502883112

Beyond species: functional diversity and the maintenance of ecological processes and services: Functional diversity in ecology and conservation
journal, August 2011


Using graph theory to analyze biological networks
journal, April 2011

  • Pavlopoulos, Georgios A.; Secrier, Maria; Moschopoulos, Charalampos N.
  • BioData Mining, Vol. 4, Issue 1
  • DOI: 10.1186/1756-0381-4-10

Alignment-free protein interaction network comparison
journal, August 2014


Community assembly: when should history matter?
journal, August 2003


Function and “functioning” in ecology: what does it mean?
journal, December 2005


Microbial diversity and metabolic networks in acid mine drainage habitats
journal, May 2015

  • Méndez-García, Celia; Peláez, Ana I.; Mesa, Victoria
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00475

Defining seasonal marine microbial community dynamics
journal, August 2011

  • Gilbert, Jack A.; Steele, Joshua A.; Caporaso, J. Gregory
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.107

Microbial community structure and its functional implications
journal, May 2009


Predicting taxonomic and functional structure of microbial communities in acid mine drainage
journal, March 2016


Proper evaluation of alignment-free network comparison methods
journal, March 2015


Fluvial network organization imprints on microbial co-occurrence networks
journal, August 2014

  • Widder, S.; Besemer, K.; Singer, G. A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 35
  • DOI: 10.1073/pnas.1411723111

Functional Molecular Ecological Networks
journal, October 2010


Community assembly: when should history matter?
journal, August 2003


An index of ecosystem diversity
journal, December 1991


Rebuilding community ecology from functional traits
journal, April 2006


Phylogenetic analysis of community assembly and structure over space and time
journal, November 2008


AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature
journal, February 2010

  • Denef, Vincent J.; Mueller, Ryan S.; Banfield, Jillian F.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.158

Defining seasonal marine microbial community dynamics
journal, August 2011

  • Gilbert, Jack A.; Steele, Joshua A.; Caporaso, J. Gregory
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.107

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

Contemporary environmental variation determines microbial diversity patterns in acid mine drainage
journal, November 2012

  • Kuang, Jia-Liang; Huang, Li-Nan; Chen, Lin-Xing
  • The ISME Journal, Vol. 7, Issue 5
  • DOI: 10.1038/ismej.2012.139

Predicting taxonomic and functional structure of microbial communities in acid mine drainage
journal, March 2016


Correlation detection strategies in microbial data sets vary widely in sensitivity and precision
journal, February 2016

  • Weiss, Sophie; Van Treuren, Will; Lozupone, Catherine
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.235

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


Toward molecular trait‐based ecology through integration of biogeochemical, geographical and metagenomic data
journal, January 2011

  • Raes, Jeroen; Letunic, Ivica; Yamada, Takuji
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.6

Microbial community structure and its functional implications
journal, May 2009


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

Molecular eco-systems biology: towards an understanding of community function
journal, June 2008

  • Raes, Jeroen; Bork, Peer
  • Nature Reviews Microbiology, Vol. 6, Issue 9
  • DOI: 10.1038/nrmicro1935

Microbial interactions: from networks to models
journal, July 2012

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

Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes
journal, February 2020


Environmental factors shape the epiphytic bacterial communities of Gracilariopsis lemaneiformis
journal, April 2021


Bacterial community assembly based on functional genes rather than species
journal, August 2011

  • Burke, C.; Steinberg, P.; Rusch, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
  • DOI: 10.1073/pnas.1101591108

Alignment-free protein interaction network comparison
journal, August 2014


Proper evaluation of alignment-free network comparison methods
journal, March 2015


Artefacts in statistical analyses of network motifs: general framework and application to metabolic networks
journal, July 2012

  • Beber, Moritz Emanuel; Fretter, Christoph; Jain, Shubham
  • Journal of The Royal Society Interface, Vol. 9, Issue 77
  • DOI: 10.1098/rsif.2012.0490

Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria
journal, April 2014

  • Barberán, Albert; Ramirez, Kelly S.; Leff, Jonathan W.
  • Ecology Letters, Vol. 17, Issue 7
  • DOI: 10.1111/ele.12282

Beyond species: functional diversity and the maintenance of ecological processes and services: Functional diversity in ecology and conservation
journal, August 2011


Species divergence and trait convergence in experimental plant community assembly
journal, December 2005


Function and “functioning” in ecology: what does it mean?
journal, December 2005


Specificity and Stability in Topology of Protein Networks
journal, May 2002


Inferring Cellular Networks Using Probabilistic Graphical Models
journal, February 2004


Microbial Biogeography: From Taxonomy to Traits
journal, May 2008


Structure and function of the global ocean microbiome
journal, May 2015


Molecular ecological network analyses
journal, January 2012


Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory
journal, January 2007


Using graph theory to analyze biological networks
journal, April 2011

  • Pavlopoulos, Georgios A.; Secrier, Maria; Moschopoulos, Charalampos N.
  • BioData Mining, Vol. 4, Issue 1
  • DOI: 10.1186/1756-0381-4-10

Inferring Correlation Networks from Genomic Survey Data
journal, September 2012


Species Co-Occurrence: a Meta-Analysis of j. m. Diamond'S Assembly Rules Model
journal, August 2002


Phylogenetic diversity promotes ecosystem stability
journal, August 2012

  • Cadotte, Marc W.; Dinnage, Russell; Tilman, David
  • Ecology, Vol. 93, Issue sp8
  • DOI: 10.1890/11-0426.1

Community structure of marine bacterioplankton: patterns, networks, and relationships to function
journal, September 2008

  • Fuhrman, Ja; Steele, Ja
  • Aquatic Microbial Ecology, Vol. 53
  • DOI: 10.3354/ame01222

Microbial diversity and metabolic networks in acid mine drainage habitats
journal, May 2015

  • Méndez-García, Celia; Peláez, Ana I.; Mesa, Victoria
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00475

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

  • Chaffron, S.; Rehrauer, H.; Pernthaler, J.
  • Cold Spring Harbor Laboratory Press
  • DOI: 10.5167/uzh-34788

Works referencing / citing this record:

Taxonomic and Functional Differences between Microbial Communities in Qinghai Lake and Its Input Streams
journal, November 2017


Taxonomic and Functional Differences between Microbial Communities in Qinghai Lake and Its Input Streams
journal, November 2017