Genetic correlation network prediction of forest soil microbial functional organization

Ma, Bin; Zhao, Kankan; Lv, Xiaofei; Su, Weiqin; Dai, Zhongmin; Gilbert, Jack A.; Brookes, Philip C.; Faust, Karoline; Xu, Jianming

doi:10.1038/s41396-018-0232-8

Title: Genetic correlation network prediction of forest soil microbial functional organization

Journal Article · Wed Jul 25 00:00:00 EDT 2018 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-018-0232-8· OSTI ID:1489668

Ma, Bin ^[1]; Zhao, Kankan ^[1]; Lv, Xiaofei ^[1]; Su, Weiqin ^[1]; Dai, Zhongmin ^[1]; Gilbert, Jack A. ^[2]; Brookes, Philip C. ^[1];

^[3]; Xu, Jianming ^[1]

Zhejiang Univ., Hangzhou (China).; Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Hangzhou (China)
Univ. of Chicago, IL (United States); Argonne National Lab. (ANL), Lemont, IL (United States)
Katholieke Univ. Leuven, Heverlee (Belgium)

Soil ecological functions are largely determined by the activities of soil microorganisms, which, in turn, are regulated by relevant interactions between genes and their corresponding pathways. Therefore, the genetic network can theoretically elucidate the functional organization that supports complex microbial community functions, although this has not been previously attempted. We generated a genetic correlation network based on 5421 genes derived from metagenomes of forest soils, identifying 7191 positive and 123 negative correlation relationships. This network consisted of 27 clusters enriched with sets of genes within speci fi c functions, represented with corresponding cluster hubs. The clusters revealed a hierarchical architecture, re fl ecting the functional organization in the soil metagenomes. Positive correlations mapped functional associations, whereas negative correlations often mapped regulatory processes. The potential functions of uncharacterized genes were predicted based on the functions of located clusters. The global genetic correlation network highlights the functional organization in soil metagenomes and provides a resource for predicting gene functions. We anticipate that the genetic correlation network may be exploited to comprehensively decipher soil microbial commu

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Natural Science Foundation of China (NSFC); Fundamental Research Funds for the Central Universities; USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1489668

Journal Information:: The ISME Journal, Vol. 12, Issue 10; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 48 works

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References (68)

Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
Metabolic network analysis of the causes and evolution of enzyme dispensability in yeast Papp, Balázs; Pál, Csaba; Hurst, Laurence D. Nature, Vol. 429, Issue 6992 https://doi.org/10.1038/nature02636	journal	June 2004
Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria Schuchmann, Kai; Müller, Volker Nature Reviews Microbiology, Vol. 12, Issue 12 https://doi.org/10.1038/nrmicro3365	journal	November 2014
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
Network deconvolution as a general method to distinguish direct dependencies in networks Feizi, Soheil; Marbach, Daniel; Médard, Muriel Nature Biotechnology, Vol. 31, Issue 8 https://doi.org/10.1038/nbt.2635	journal	July 2013
A genetic interaction network of five genes for human polycystic kidney and liver diseases defines polycystin-1 as the central determinant of cyst formation Fedeles, Sorin V.; Tian, Xin; Gallagher, Anna-Rachel Nature Genetics, Vol. 43, Issue 7 https://doi.org/10.1038/ng.860	journal	June 2011
Fast unfolding of communities in large networks Blondel, Vincent D.; Guillaume, Jean-Loup; Lambiotte, Renaud Journal of Statistical Mechanics: Theory and Experiment, Vol. 2008, Issue 10 https://doi.org/10.1088/1742-5468/2008/10/P10008	journal	October 2008
Adaptive linear step-up procedures that control the false discovery rate Benjamini, Yoav; Krieger, Abba M.; Yekutieli, Daniel Biometrika, Vol. 93, Issue 3 https://doi.org/10.1093/biomet/93.3.491	journal	September 2006
Fe–S proteins that regulate gene expression Mettert, Erin L.; Kiley, Patricia J. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2014.11.018	journal	June 2015
Environmental and genetic perturbations reveal different networks of metabolic regulation Greenberg, Anthony J.; Hackett, Sean R.; Harshman, Lawrence G. Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.96	journal	January 2011
Controllability analysis of the directed human protein interaction network identifies disease genes and drug targets Vinayagam, Arunachalam; Gibson, Travis E.; Lee, Ho-Joon Proceedings of the National Academy of Sciences, Vol. 113, Issue 18 https://doi.org/10.1073/pnas.1603992113	journal	April 2016
Genetic interaction networks: better understand to better predict Boucher, Benjamin; Jenna, Sarah Frontiers in Genetics, Vol. 4 https://doi.org/10.3389/fgene.2013.00290	journal	January 2013
Transmembrane glycine zippers: Physiological and pathological roles in membrane proteins Kim, S.; Jeon, T. -J.; Oberai, A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 40 https://doi.org/10.1073/pnas.0501234102	journal	September 2005
Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States Fierer, N.; Ladau, J.; Clemente, J. C. Science, Vol. 342, Issue 6158 https://doi.org/10.1126/science.1243768	journal	October 2013
Network-Thinking: Graphs to Analyze Microbial Complexity and Evolution Corel, Eduardo; Lopez, Philippe; Méheust, Raphaël Trends in Microbiology, Vol. 24, Issue 3 https://doi.org/10.1016/j.tim.2015.12.003	journal	March 2016
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
A global genetic interaction network maps a wiring diagram of cellular function Costanzo, M.; VanderSluis, B.; Koch, E. N. Science, Vol. 353, Issue 6306 https://doi.org/10.1126/science.aaf1420	journal	September 2016
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
The Genetic Landscape of a Cell Costanzo, M.; Baryshnikova, A.; Bellay, J. Science, Vol. 327, Issue 5964 https://doi.org/10.1126/science.1180823	journal	January 2010
Systems genetics of complex traits in Drosophila melanogaster Ayroles, Julien F.; Carbone, Mary Anna; Stone, Eric A. Nature Genetics, Vol. 41, Issue 3 https://doi.org/10.1038/ng.332	journal	February 2009
Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China Ma, Bin; Wang, Haizhen; Dsouza, Melissa The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2015.261	journal	January 2016
Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’ Brewer, Tess E.; Handley, Kim M.; Carini, Paul Nature Microbiology, Vol. 2, Issue 2 https://doi.org/10.1038/nmicrobiol.2016.198	journal	October 2016
Hierarchical Modularity and the Evolution of Genetic Interactomes across Species Ryan, Colm J.; Roguev, Assen; Patrick, Kristin Molecular Cell, Vol. 46, Issue 5 https://doi.org/10.1016/j.molcel.2012.05.028	journal	June 2012
CLARK: fast and accurate classification of metagenomic and genomic sequences using discriminative k-mers Ounit, Rachid; Wanamaker, Steve; Close, Timothy J. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1419-2	journal	March 2015
Defining genetic interaction Mani, R.; St. Onge, R. P.; Hartman, J. L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 9 https://doi.org/10.1073/pnas.0712255105	journal	February 2008
Cross-biome metagenomic analyses of soil microbial communities and their functional attributes Fierer, N.; Leff, J. W.; Adams, B. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 52 https://doi.org/10.1073/pnas.1215210110	journal	December 2012
Computational Improvements Reveal Great Bacterial Diversity and High Metal Toxicity in Soil Gans, J. Science, Vol. 309, Issue 5739 https://doi.org/10.1126/science.1112665	journal	August 2005
Flexible C : N ratio enhances metabolism of large phytoplankton when resource supply is intermittent Talmy, D.; Blackford, J.; Hardman-Mountford, N. J. Biogeosciences, Vol. 11, Issue 17 https://doi.org/10.5194/bg-11-4881-2014	journal	January 2014
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Molecular ecological network analyses Deng, Ye; Jiang, Yi-Huei; Yang, Yunfeng BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-113	journal	January 2012
Long-term phenotypic evolution of bacteria Plata, Germán; Henry, Christopher S.; Vitkup, Dennis Nature, Vol. 517, Issue 7534 https://doi.org/10.1038/nature13827	journal	October 2014
Evolutionary constraints on hub and non-hub proteins in human protein interaction network: Insight from protein connectivity and intrinsic disorder Manna, Baisali; Bhattacharya, Tanusree; Kahali, Bratati Gene, Vol. 434, Issue 1-2 https://doi.org/10.1016/j.gene.2008.12.013	journal	April 2009
Crystal structure of the ribosomal protein S6 from Thermus thermophilus. Lindahl, M.; Svensson, L. A.; Liljas, A. The EMBO Journal, Vol. 13, Issue 6 https://doi.org/10.1002/j.1460-2075.1994.tb06376.x	journal	March 1994
Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology Prosser, James I. Nature Reviews Microbiology, Vol. 13, Issue 7 https://doi.org/10.1038/nrmicro3468	journal	June 2015
X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution Peters, J. W. Science, Vol. 282, Issue 5395 https://doi.org/10.1126/science.282.5395.1853	journal	December 1998
Functional Gene Composition, Diversity and Redundancy in Microbial Stream Biofilm Communities Dopheide, Andrew; Lear, Gavin; He, Zhili PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0123179	journal	April 2015
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Global diversity and geography of soil fungi Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei Science, Vol. 346, Issue 6213 https://doi.org/10.1126/science.1256688	journal	November 2014
QuickGO: a web-based tool for Gene Ontology searching Binns, D.; Dimmer, E.; Huntley, R. Bioinformatics, Vol. 25, Issue 22 https://doi.org/10.1093/bioinformatics/btp536	journal	September 2009
Wisdom of crowds for robust gene network inference Marbach, Daniel; Costello, James C.; Küffner, Robert Nature Methods, Vol. 9, Issue 8 https://doi.org/10.1038/nmeth.2016	journal	July 2012
Global Mapping of the Yeast Genetic Interaction Network Tong, A. H. Y. Science, Vol. 303, Issue 5659 https://doi.org/10.1126/science.1091317	journal	February 2004
Using network analysis to explore co-occurrence patterns in soil microbial communities Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O. The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.119	journal	September 2011
Information theory perspective on network robustness Schieber, Tiago A.; Carpi, Laura; Frery, Alejandro C. Physics Letters A, Vol. 380, Issue 3 https://doi.org/10.1016/j.physleta.2015.10.055	journal	January 2016
Genomes from Metagenomics Sharon, I.; Banfield, J. F. Science, Vol. 342, Issue 6162 https://doi.org/10.1126/science.1247023	journal	November 2013
Microbial interactions and community assembly at microscales Cordero, Otto X.; Datta, Manoshi S. Current Opinion in Microbiology, Vol. 31 https://doi.org/10.1016/j.mib.2016.03.015	journal	June 2016
Horizontal Gene Transfer in Prokaryotes: Quantification and Classification Koonin, Eugene V.; Makarova, Kira S.; Aravind, L. Annual Review of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.micro.55.1.709	journal	October 2001
MetaQUAST: evaluation of metagenome assemblies Mikheenko, Alla; Saveliev, Vladislav; Gurevich, Alexey Bioinformatics, Vol. 32, Issue 7 https://doi.org/10.1093/bioinformatics/btv697	journal	November 2015
One gram of soil: a microbial biochemical gene library Trevors, J. T. Antonie van Leeuwenhoek, Vol. 97, Issue 2 https://doi.org/10.1007/s10482-009-9397-5	journal	November 2009
The diversity and biogeography of soil bacterial communities Fierer, N.; Jackson, R. B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0507535103	journal	January 2006
Software for pre-processing Illumina next-generation sequencing short read sequences Chen, Chuming; Khaleel, Sari S.; Huang, Hongzhan Source Code for Biology and Medicine, Vol. 9, Issue 1 https://doi.org/10.1186/1751-0473-9-8	journal	May 2014
Spatial scale drives patterns in soil bacterial diversity: Spatial scale drives soil diversity O'Brien, Sarah L.; Gibbons, Sean M.; Owens, Sarah M. Environmental Microbiology, Vol. 18, Issue 6 https://doi.org/10.1111/1462-2920.13231	journal	March 2016
Protein interaction networks from yeast to human Bork, Peer; Jensen, Lars J.; von Mering, Christian Current Opinion in Structural Biology, Vol. 14, Issue 3 https://doi.org/10.1016/j.sbi.2004.05.003	journal	June 2004
Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions Mistry, Jaina; Finn, Robert D.; Eddy, Sean R. Nucleic Acids Research, Vol. 41, Issue 12 https://doi.org/10.1093/nar/gkt263	journal	April 2013
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Evolution of biomolecular networks — lessons from metabolic and protein interactions Yamada, Takuji; Bork, Peer Nature Reviews Molecular Cell Biology, Vol. 10, Issue 11 https://doi.org/10.1038/nrm2787	journal	November 2009
The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages Shi, Shengjing; Nuccio, Erin E.; Shi, Zhou J. Ecology Letters, Vol. 19, Issue 8 https://doi.org/10.1111/ele.12630	journal	June 2016
Biological interaction networks are conserved at the module level Zinman, Guy E.; Zhong, Shan; Bar-Joseph, Ziv BMC Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1752-0509-5-134	journal	January 2011
Gene co-expression network analysis reveals common system-level properties of prognostic genes across cancer types Yang, Yang; Han, Leng; Yuan, Yuan Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4231	journal	February 2014
Flexible C : N ratio enhances metabolism of large phytoplankton when resource supply is intermittent Talmy, D.; Blackford, J.; Hardman-Mountford, N. J. Biogeosciences Discussions, Vol. 11, Issue 4 https://doi.org/10.5194/bgd-11-5179-2014	journal	January 2014
Dynamics of collective action to conserve a large common-pool resource Andersson, David; Bratsberg, Sigrid; Ringsmuth, Andrew K. Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-87109-x	journal	April 2021
Erratum: Using network analysis to explore co-occurrence patterns in soil microbial communities Barberán, Albert; Bates, Scott T.; Casamayor, Emilio O. The ISME Journal, Vol. 8, Issue 4 https://doi.org/10.1038/ismej.2013.236	journal	March 2014
First principles of terrestrial life: exemplars for potential extra-terrestrial biology von Hegner, Ian Theory in Biosciences, Vol. 141, Issue 3 https://doi.org/10.1007/s12064-022-00373-x	journal	July 2022
Microbial diversity and function in soil: from genes to ecosystems Torsvik, Vigdis; Øvreås, Lise Current Opinion in Microbiology, Vol. 5, Issue 3, p. 240-245 https://doi.org/10.1016/s1369-5274(02)00324-7	journal	June 2002
Targeted A-to-G base editing of chloroplast DNA in plants Mok, Young Geun; Hong, Sunghyun; Bae, Su-Ji Nature Plants, Vol. 8, Issue 12 https://doi.org/10.1038/s41477-022-01279-8	journal	December 2022
A study of associations between CUBN, HNF1A, and LIPC gene polymorphisms and coronary artery disease Park, Han Sung; Kim, In Jai; Kim, Eun Gyo Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-73048-6	journal	October 2020
Potassium Uptake Modulates Staphylococcus aureus Metabolism Gries, Casey M.; Sadykov, Marat R.; Bulock, Logan L. mSphere, Vol. 1, Issue 3 https://doi.org/10.1128/msphere.00125-16	journal	June 2016
MetaVelvet-DL: a MetaVelvet deep learning extension for de novo metagenome assembly Liang, Kuo-ching; Sakakibara, Yasubumi BMC Bioinformatics, Vol. 22, Issue S6 https://doi.org/10.1186/s12859-020-03737-6	journal	June 2021
Mutualism, Facilitation, and the Structure of Ecological Communities Stachowicz, John J. BioScience, Vol. 51, Issue 3 https://doi.org/10.1641/0006-3568(2001)051[0235:mfatso]2.0.co;2	journal	January 2001

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