The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales

Li, Hong-Yi; Wang, Hang; Wang, Hai-Tao; Xin, Pei-Yong; Xu, Xin-Hua; Ma, Yun; Liu, Wei-Ping; Teng, Chang-Yun; Jiang, Cheng-Liang; Lou, Li-Ping; Arnold, Wyatt; Cralle, Lauren; Zhu, Yong-Guan; Chu, Jin-Fang; Gilbert, Jack A.; Zhang, Zhi-Jian

doi:10.1186/s40168-018-0561-x

The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales

Journal Article · Fri Oct 19 00:00:00 EDT 2018 · Microbiome

DOI:https://doi.org/10.1186/s40168-018-0561-x· OSTI ID:1618944

Li, Hong-Yi; Wang, Hang; Wang, Hai-Tao; Xin, Pei-Yong; Xu, Xin-Hua; Ma, Yun; Liu, Wei-Ping; Teng, Chang-Yun; Jiang, Cheng-Liang; Lou, Li-Ping; Arnold, Wyatt; Cralle, Lauren; Zhu, Yong-Guan; Chu, Jin-Fang; Gilbert, Jack A.; Zhang, Zhi-Jian

Abstract Background

Paddy soil dissolved organic matter (DOM) represents a major hotspot for soil biogeochemistry, yet we know little about its chemodiversity let alone the microbial community that shapes it. Here, we leveraged ultrahigh-resolution mass spectrometry, amplicon, and metagenomic sequencing to characterize the molecular distribution of DOM and the taxonomic and functional microbial diversity in paddy soils across China. We hypothesized that variances in microbial community significantly associate with changes in soil DOM molecular composition.

Results

We report that both microbial and DOM profiles revealed geographic patterns that were associated with variation in mean monthly precipitation, mean annual temperature, and pH. DOM molecular diversity was significantly correlated with microbial taxonomic diversity. An increase in DOM molecules categorized as peptides, carbohydrates, and unsaturated aliphatics, and a decrease in those belonging to polyphenolics and polycyclic aromatics, significantly correlated with proportional changes in some of the microbial taxa, such as Syntrophobacterales , Thermoleophilia , Geobacter , Spirochaeta , Gaiella , and Defluviicoccus . DOM composition was also associated with the relative abundances of the microbial metabolic pathways, such as anaerobic carbon fixation, glycolysis, lignolysis, fermentation, and methanogenesis.

Conclusions

Our study demonstrates the continental-scale distribution of DOM is significantly correlated with the taxonomic profile and metabolic potential of the rice paddy microbiome. Abiotic factors that have a distinct effect on community structure can also influence the chemodiversity of DOM and vice versa. Deciphering these associations and the underlying mechanisms can precipitate understanding of the complex ecology of paddy soils, as well as help assess the effects of human activities on biogeochemistry and greenhouse gas emissions in paddy soils.

View Journal Article

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

Sponsoring Organization:: National Natural Science Foundation of China; USDOE; Zhejiang Science and Technology Innovation Program

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1618944

Alternate ID(s):: OSTI ID: 1627049

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 6; ISSN 2049-2618

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (75)

From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter Koch, B. P.; Dittmar, T. Rapid Communications in Mass Spectrometry, Vol. 20, Issue 5 https://doi.org/10.1002/rcm.2386	journal	February 2006
Substrate flow in the rhizosphere Lynch, J. M.; Whipps, J. M. Plant and Soil, Vol. 129, Issue 1 https://doi.org/10.1007/BF00011685	journal	December 1990
The heterogeneous nature of microbial products as shown by solid-state13C CP/MAS NMR spectroscopy Golchin, A.; Clarke, P.; Oades, J. M. Biogeochemistry, Vol. 34, Issue 2 https://doi.org/10.1007/BF02180974	journal	August 1996
Molecular characterization of dissolved organic matter (DOM): a critical review Nebbioso, Antonio; Piccolo, Alessandro Analytical and Bioanalytical Chemistry, Vol. 405, Issue 1 https://doi.org/10.1007/s00216-012-6363-2	journal	September 2012
Comparative study of organic matter chemical characterization using negative and positive mode electrospray ionization ultrahigh-resolution mass spectrometry Ohno, Tsutomu; Sleighter, Rachel L.; Hatcher, Patrick G. Analytical and Bioanalytical Chemistry, Vol. 408, Issue 10 https://doi.org/10.1007/s00216-016-9346-x	journal	February 2016
Pesticide effects on bacterial diversity in agricultural soils - a review Johnsen, Kaare; Jacobsen, Carsten; Torsvik, Vigdis Biology and Fertility of Soils, Vol. 33, Issue 6 https://doi.org/10.1007/s003740100351	journal	June 2001
Linking dissolved organic carbon cycling to organic carbon fluxes in rice paddies under different water management practices Said-Pullicino, Daniel; Miniotti, Eleonora F.; Sodano, Marcella Plant and Soil, Vol. 401, Issue 1-2 https://doi.org/10.1007/s11104-015-2751-7	journal	November 2015
Bacterial succession in paddy soils derived from different parent materials Sheng, Rong; Qin, Hongling; O’Donnell, Anthony G. Journal of Soils and Sediments, Vol. 15, Issue 4 https://doi.org/10.1007/s11368-014-1058-2	journal	January 2015
Factors affecting methane emission from rice fields Neue, H. U.; Wassmann, R.; Lantin, R. S. Atmospheric Environment, Vol. 30, Issue 10-11 https://doi.org/10.1016/1352-2310(95)00375-4	journal	May 1996
Geobacter Lovley, Derek R.; Ueki, Toshiyuki; Zhang, Tian Advances in Microbial Physiology https://doi.org/10.1016/B978-0-12-387661-4.00004-5	book	January 2011
The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter Kögel-Knabner, I. Soil Biology and Biochemistry, Vol. 34, Issue 2 https://doi.org/10.1016/S0038-0717(01)00158-4	journal	February 2002
Changes in soil microbial community composition in response to fertilization of paddy soils in subtropical China Dong, Wen-Yi; Zhang, Xin-Yu; Dai, Xiao-Qin Applied Soil Ecology, Vol. 84 https://doi.org/10.1016/j.apsoil.2014.06.007	journal	December 2014
Biogeochemistry of paddy soils Kögel-Knabner, Ingrid; Amelung, Wulf; Cao, Zhihong Geoderma, Vol. 157, Issue 1-2 https://doi.org/10.1016/j.geoderma.2010.03.009	journal	June 2010
Probing molecular-level transformations of dissolved organic matter: insights on photochemical degradation and protozoan modification of DOM from electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry Kujawinski, Elizabeth B.; Del Vecchio, Rossana; Blough, Neil V. Marine Chemistry, Vol. 92, Issue 1-4 https://doi.org/10.1016/j.marchem.2004.06.038	journal	December 2004
Concentration dynamics and biodegradability of dissolved organic matter in wetland soils subjected to experimental warming Wang, Hang; Holden, Joseph; Zhang, ZhiJian Science of The Total Environment, Vol. 470-471 https://doi.org/10.1016/j.scitotenv.2013.10.049	journal	February 2014
Comparing molecular composition of dissolved organic matter in soil and stream water: Influence of land use and chemical characteristics Seifert, Anne-Gret; Roth, Vanessa-Nina; Dittmar, Thorsten Science of The Total Environment, Vol. 571 https://doi.org/10.1016/j.scitotenv.2016.07.033	journal	November 2016
Effect of past peat cultivation practices on present dynamics of dissolved organic carbon Frank, S.; Tiemeyer, B.; Bechtold, M. Science of The Total Environment, Vol. 574 https://doi.org/10.1016/j.scitotenv.2016.07.121	journal	January 2017
Paddy soil microbial communities driven by environment- and microbe-microbe interactions: A case study of elevation-resolved microbial communities in a rice terrace Sun, Weimin; Xiao, Enzong; Pu, Zilun Science of The Total Environment, Vol. 612 https://doi.org/10.1016/j.scitotenv.2017.08.275	journal	January 2018
Does the chemical nature of soil carbon drive the structure and functioning of soil microbial communities? Ng, E. -L.; Patti, A. F.; Rose, M. T. Soil Biology and Biochemistry, Vol. 70 https://doi.org/10.1016/j.soilbio.2013.12.004	journal	March 2014
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices Li, Dinghua; Luo, Ruibang; Liu, Chi-Man Methods, Vol. 102 https://doi.org/10.1016/j.ymeth.2016.02.020	journal	June 2016
Fundamentals of Molecular Formula Assignment to Ultrahigh Resolution Mass Data of Natural Organic Matter Koch, Boris P.; Dittmar, Thorsten; Witt, Matthias Analytical Chemistry, Vol. 79, Issue 4 https://doi.org/10.1021/ac061949s	journal	February 2007
Molecular Chemodiversity of Dissolved Organic Matter in Paddy Soils Li, Xiao-Ming; Sun, Guo-Xin; Chen, Song-Can Environmental Science & Technology, Vol. 52, Issue 3 https://doi.org/10.1021/acs.est.7b00377	journal	January 2018
Investigation on Temporal Variation in Methane Emission from Different Rice Cultivars under the Influence of Weeds Tyagi, Larisha; Verma, Amitosh; Singh, S. N. Environmental Monitoring and Assessment, Vol. 93, Issue 1-3 https://doi.org/10.1023/B:EMAS.0000016793.13260.6e	journal	April 2004
Farming the planet: 2. Geographic distribution of crop areas, yields, physiological types, and net primary production in the year 2000: GLOBAL CROP AREAS AND YIELDS IN 2000 Monfreda, Chad; Ramankutty, Navin; Foley, Jonathan A. Global Biogeochemical Cycles, Vol. 22, Issue 1 https://doi.org/10.1029/2007GB002947	journal	March 2008
Humic substances as electron acceptors for microbial respiration Lovley, Derek R.; Coates, John D.; Blunt-Harris, Elizabeth L. Nature, Vol. 382, Issue 6590 https://doi.org/10.1038/382445a0	journal	August 1996
Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing Hori, Tomoyuki; Müller, Alexandra; Igarashi, Yasuo The ISME Journal, Vol. 4, Issue 2 https://doi.org/10.1038/ismej.2009.100	journal	September 2009
Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system Osterholz, Helena; Singer, Gabriel; Wemheuer, Bernd The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.231	journal	January 2016
The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen Baughn, Anthony D.; Malamy, Michael H. Nature, Vol. 427, Issue 6973 https://doi.org/10.1038/nature02285	journal	January 2004
Extracellular electron transfer via microbial nanowires Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena Nature, Vol. 435, Issue 7045, p. 1098-1101 https://doi.org/10.1038/nature03661	journal	June 2005
The contentious nature of soil organic matter Lehmann, Johannes; Kleber, Markus Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature16069	journal	November 2015
Groundwater–surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover Stegen, James C.; Fredrickson, James K.; Wilkins, Michael J. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11237	journal	April 2016
Fast and sensitive taxonomic classification for metagenomics with Kaiju Menzel, Peter; Ng, Kim Lee; Krogh, Anders Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11257	journal	April 2016
Temperature mediates continental-scale diversity of microbes in forest soils Zhou, Jizhong; Deng, Ye; Shen, Lina Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12083	journal	July 2016
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13630	journal	November 2016
Chemodiversity of dissolved organic matter in lakes driven by climate and hydrology Kellerman, Anne M.; Dittmar, Thorsten; Kothawala, Dolly N. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4804	journal	May 2014
The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate Jing, Xin; Sanders, Nathan J.; Shi, Yu Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9159	journal	September 2015
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Beyond biogeographic patterns: processes shaping the microbial landscape Hanson, China A.; Fuhrman, Jed A.; Horner-Devine, M. Claire Nature Reviews Microbiology, Vol. 10, Issue 7 https://doi.org/10.1038/nrmicro2795	journal	May 2012
Cytochrome cbb3 oxidase and bacterial microaerobic metabolism Pitcher, R. S.; Brittain, T.; Watmugh, N. J. Biochemical Society Transactions, Vol. 30, Issue 4 https://doi.org/10.1042/bst0300653	journal	August 2002
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
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Caporaso, J. G.; Lauber, C. L.; Walters, W. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000080107	journal	June 2010
Iron traps terrestrially derived dissolved organic matter at redox interfaces Riedel, T.; Zak, D.; Biester, H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 25 https://doi.org/10.1073/pnas.1221487110	journal	June 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
RNA-Seq gene expression estimation with read mapping uncertainty Li, Bo; Ruotti, Victor; Stewart, Ron M. Bioinformatics, Vol. 26, Issue 4 https://doi.org/10.1093/bioinformatics/btp692	journal	December 2009
Associating microbiome composition with environmental covariates using generalized UniFrac distances Chen, Jun; Bittinger, Kyle; Charlson, Emily S. Bioinformatics, Vol. 28, Issue 16 https://doi.org/10.1093/bioinformatics/bts342	journal	June 2012
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data: Fig. 1. Aßhauer, Kathrin P.; Wemheuer, Bernd; Daniel, Rolf Bioinformatics, Vol. 31, Issue 17 https://doi.org/10.1093/bioinformatics/btv287	journal	May 2015
KEGG: Kyoto Encyclopedia of Genes and Genomes Ogata, H.; Goto, S.; Sato, K. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.29	journal	January 1999
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
TIGRFAMs and Genome Properties in 2013 Haft, Daniel H.; Selengut, Jeremy D.; Richter, Roland A. Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1234	journal	November 2012
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
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
FOAM (Functional Ontology Assignments for Metagenomes): a Hidden Markov Model (HMM) database with environmental focus Prestat, Emmanuel; David, Maude M.; Hultman, Jenni Nucleic Acids Research, Vol. 42, Issue 19 https://doi.org/10.1093/nar/gku702	journal	September 2014
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
Controls on the Dynamics of Dissolved Organic Matter in Soils: a Review Kalbitz, K.; Solinger, S.; Park, J. -H. Soil Science, Vol. 165, Issue 4 https://doi.org/10.1097/00010694-200004000-00001	journal	January 2000
Dynamics of the methanogenic archaeal community in anoxic rice soil upon addition of straw Conrad, R.; Klose, M. European Journal of Soil Science, Vol. 57, Issue 4 https://doi.org/10.1111/j.1365-2389.2006.00791.x	journal	August 2006
Succession of bacterial community structure and diversity in a paddy soil oxygen gradient Noll, Matthias; Matthies, Diethart; Frenzel, Peter Environmental Microbiology, Vol. 7, Issue 3 https://doi.org/10.1111/j.1462-2920.2005.00700.x	journal	March 2005
Root-induced iron oxidation and pH changes in the lowland rice rhizosphere Begg, C. B. M.; Kirk, G. J. D.; Mackenzie, A. F. New Phytologist, Vol. 128, Issue 3 https://doi.org/10.1111/j.1469-8137.1994.tb02993.x	journal	November 1994
Microbiology of flooded rice paddies Liesack, Werner; Schnell, Sylvia; Revsbech, Niels Peter FEMS Microbiology Reviews, Vol. 24, Issue 5 https://doi.org/10.1111/j.1574-6976.2000.tb00563.x	journal	December 2000
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria Summers, Z. M.; Fogarty, H. E.; Leang, C. Science, Vol. 330, Issue 6009, p. 1413-1415 https://doi.org/10.1126/science.1196526	journal	December 2010
Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils Holmes, Dawn E.; Shrestha, Pravin M.; Walker, David J. F. Applied and Environmental Microbiology, Vol. 83, Issue 9 https://doi.org/10.1128/AEM.00223-17	journal	March 2017
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
Feed in summer, rest in winter: microbial carbon utilization in forest topsoil Žifčáková, Lucia; Větrovský, Tomáš; Lombard, Vincent Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0340-0	journal	September 2017
Effects of Land Use Changes from Paddy Fields on Soil Bacterial Communities in a Hilly and Mountainous Area Rokunuzzaman, Md; Ueda, Yumiko; Chen, Li Microbes and environments, Vol. 31, Issue 2 https://doi.org/10.1264/jsme2.ME15187	journal	January 2016
Metabolic Reconstruction for Metagenomic Data and Its Application to the Human Microbiome Abubucker, Sahar; Segata, Nicola; Goll, Johannes PLoS Computational Biology, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pcbi.1002358	journal	June 2012
Hailstones: A Window into the Microbial and Chemical Inventory of a Storm Cloud Šantl-Temkiv, Tina; Finster, Kai; Dittmar, Thorsten PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053550	journal	January 2013
The Molecular Composition of Dissolved Organic Matter in Forest Soils as a Function of pH and Temperature Roth, Vanessa-Nina; Dittmar, Thorsten; Gaupp, Reinhard PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0119188	journal	March 2015
Microbial Community Structure Affects Marine Dissolved Organic Matter Composition Kujawinski, Elizabeth B.; Longnecker, Krista; Barott, Katie L. Frontiers in Marine Science, Vol. 3 https://doi.org/10.3389/fmars.2016.00045	journal	April 2016
Age, turnover and molecular diversity of soil organic matter in aggregates of a Gleysol Monreal, C. M.; Schulten, H. -R.; Kodama, H. Canadian Journal of Soil Science, Vol. 77, Issue 3 https://doi.org/10.4141/S95-064	journal	August 1997
Nitrogen export from a boreal stream network following forest harvesting: seasonal nitrate removal and conservative export of organic forms Schelker, J.; Sponseller, R.; Ring, E. Biogeosciences, Vol. 13, Issue 1 https://doi.org/10.5194/bg-13-1-2016	journal	January 2016

Similar Records

Challenges in integrating dissolved organic matter chemodiversity into kinetic models of soil respiration

Journal Article · Wed Aug 27 20:00:00 EDT 2025 · Soil Biology and Biochemistry · OSTI ID:3000088

Host-specific and tissue-dependent orchestration of microbiome community structure in traditional rice paddy ecosystems

Journal Article · Tue Jun 02 00:00:00 EDT 2020 · Plant and Soil · OSTI ID:1803329

Related Subjects

Microbiology

The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales

Citation Formats

References (75)

Similar Records

Related Subjects