Expression of macromolecular organic nitrogen degrading enzymes identifies potential mediators of soil organic N availability to an annual grass

Sieradzki, Ella T.; Nuccio, Erin E.; Pett-Ridge, Jennifer; Firestone, Mary K.

doi:10.1038/s41396-023-01402-3

Title: Expression of macromolecular organic nitrogen degrading enzymes identifies potential mediators of soil organic N availability to an annual grass

Journal Article · 14 April 2023 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-023-01402-3 · OSTI ID:1970056

;

; Firestone, Mary K.

Abstract Nitrogen (N) is frequently limiting to plant growth, in part because most soil N is present as polymeric organic compounds that are not readily taken up by plants. Microbial depolymerization of these large macromolecular N-substrates gradually releases available inorganic N. While many studies have researched and modeled controls on soil organic matter formation and bulk N mineralization, the ecological—spatial, temporal and phylogenetic—patterns underlying organic N degradation remain unclear. We analyzed 48 time-resolved metatranscriptomes and quantified N-depolymerization gene expression to resolve differential expression by soil habitat and time in specific taxonomic groups and gene-based guilds. We observed much higher expression of extracellular serine-type proteases than other extracellular N-degrading enzymes, with protease expression of predatory bacteria declining with time and other taxonomic patterns driven by the presence (Gammaproteobacteria) or absence (Thermoproteota) of live roots and root detritus (Deltaproteobacteria and Fungi). The primary chitinase chit1 gene was more highly expressed by eukaryotes near root detritus, suggesting predation of fungi. In some lineages, increased gene expression over time suggests increased competitiveness with rhizosphere age (Chloroflexi). Phylotypes from some genera had protease expression patterns that could benefit plant N nutrition, for example, we identified a Janthinobacterium phylotype and two Burkholderiales that depolymerize organic N near young roots and a Rhizobacter with elevated protease levels near mature roots. These taxon-resolved gene expression results provide an ecological read-out of microbial interactions and controls on N dynamics in specific soil microhabitats and could be used to target potential plant N bioaugmentation strategies.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: NONE; SC0020163; SC0016247

OSTI ID:: 1970056

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 7 Vol. 17; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (73)

The structure and synthesis of the fungal cell wall Bowman, Shaun M.; Free, Stephen J. BioEssays, Vol. 28, Issue 8 https://doi.org/10.1002/bies.20441	journal	January 2006
Activity‐Based Protein Profiling of Chitin Catabolism Zegeye, Elias K.; Sadler, Natalie C.; Lomas, Gerard X. ChemBioChem, Vol. 22, Issue 4 https://doi.org/10.1002/cbic.202000616	journal	November 2020
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Rhizosphere Carbon Turnover from Cradle to Grave: The Role of Microbe–Plant Interactions Pett-Ridge, Jennifer; Shi, Shengjing; Estera-Molina, Katerina Rhizosphere Biology: Interactions Between Microbes and Plants https://doi.org/10.1007/978-981-15-6125-2_2	book	August 2020
Nitrogen limitation on land and in the sea: How can it occur? Vitousek, PeterM.; Howarth, RobertW. Biogeochemistry, Vol. 13, Issue 2 https://doi.org/10.1007/BF00002772	journal	January 1991
Plant and soil nitrogen dynamics in California annual grassland Jackson, L. E.; Strauss, R. B.; Firestone, M. K. Plant and Soil, Vol. 110, Issue 1 https://doi.org/10.1007/BF02143533	journal	August 1988
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review Blagodatskaya, Е.; Kuzyakov, Y. Biology and Fertility of Soils, Vol. 45, Issue 2 https://doi.org/10.1007/s00374-008-0334-y	journal	October 2008
Soil enzyme activities and abundance of microbial functional genes involved in nitrogen transformations in an organic farming system Ouyang, Yang; Reeve, Jennifer R.; Norton, Jeanette M. Biology and Fertility of Soils, Vol. 54, Issue 4 https://doi.org/10.1007/s00374-018-1272-y	journal	March 2018
Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils Brzostek, Edward R.; Greco, Alison; Drake, John E. Biogeochemistry, Vol. 115, Issue 1-3 https://doi.org/10.1007/s10533-012-9818-9	journal	December 2012
Minerals in the rhizosphere: overlooked mediators of soil nitrogen availability to plants and microbes Jilling, Andrea; Keiluweit, Marco; Contosta, Alexandra R. Biogeochemistry, Vol. 139, Issue 2 https://doi.org/10.1007/s10533-018-0459-5	journal	June 2018
A holistic framework integrating plant-microbe-mineral regulation of soil bioavailable nitrogen Daly, Amanda B.; Jilling, Andrea; Bowles, Timothy M. Biogeochemistry, Vol. 154, Issue 2 https://doi.org/10.1007/s10533-021-00793-9	journal	May 2021
Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis Rubin, Rachel L.; van Groenigen, Kees Jan; Hungate, Bruce A. Plant and Soil, Vol. 416, Issue 1-2 https://doi.org/10.1007/s11104-017-3199-8	journal	March 2017
Priming effect of litter mineralization: the role of root exudate depends on its interactions with litter quality and soil condition Tian, Kai; Kong, Xiangshi; Yuan, Liuhuan Plant and Soil, Vol. 440, Issue 1-2 https://doi.org/10.1007/s11104-019-04070-5	journal	May 2019
Changes in soil properties rather than functional gene abundance control carbon and nitrogen mineralization rates during long-term natural revegetation Zhang, Kerong; Li, Xinshuai; Cheng, Xiaoli Plant and Soil, Vol. 443, Issue 1-2 https://doi.org/10.1007/s11104-019-04212-9	journal	August 2019
Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen Clarholm, Marianne Soil Biology and Biochemistry, Vol. 17, Issue 2 https://doi.org/10.1016/0038-0717(85)90113-0	journal	January 1985
Transformations of nitrogen Myrold, David D. Principles and Applications of Soil Microbiology https://doi.org/10.1016/B978-0-12-820202-9.00015-0	book	January 2021
Tillage changes microbial biomass and enzyme activities in particle-size fractions of a Haplic Chernozem Kandeler, E. Soil Biology and Biochemistry, Vol. 31, Issue 9 https://doi.org/10.1016/S0038-0717(99)00041-3	journal	August 1999
Proteolytic activity in soil: A review Vranova, Valerie; Rejsek, Klement; Formanek, Pavel Applied Soil Ecology, Vol. 70 https://doi.org/10.1016/j.apsoil.2013.04.003	journal	August 2013
Co-inoculation with endophytic and rhizosphere bacteria allows reduced application rates of N-fertilizer for rice plant Etesami, Hassan; Alikhani, Hossein Ali Rhizosphere, Vol. 2 https://doi.org/10.1016/j.rhisph.2016.09.003	journal	December 2016
Seasonal protein dynamics in Alaskan arctic tundra soils Weintraub, Michael N.; Schimel, Joshua P. Soil Biology and Biochemistry, Vol. 37, Issue 8 https://doi.org/10.1016/j.soilbio.2005.01.005	journal	August 2005
Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes Wallenstein, Matthew D.; Weintraub, Michael N. Soil Biology and Biochemistry, Vol. 40, Issue 9 https://doi.org/10.1016/j.soilbio.2008.01.024	journal	September 2008
Carbon-to-nitrogen ratio is a poor predictor of low molecular weight organic nitrogen mineralization in soil Roberts, P.; Stockdale, R.; Khalid, M. Soil Biology and Biochemistry, Vol. 41, Issue 8 https://doi.org/10.1016/j.soilbio.2009.04.020	journal	August 2009
Protein breakdown represents a major bottleneck in nitrogen cycling in grassland soils Jan, M. T.; Roberts, P.; Tonheim, S. K. Soil Biology and Biochemistry, Vol. 41, Issue 11 https://doi.org/10.1016/j.soilbio.2009.08.013	journal	November 2009
Determination of gross rates of amino acid production and immobilization in decomposing leaf litter by a novel 15N isotope pool dilution technique Wanek, Wolfgang; Mooshammer, Maria; Blöchl, Andreas Soil Biology and Biochemistry, Vol. 42, Issue 8 https://doi.org/10.1016/j.soilbio.2010.04.001	journal	August 2010
Microbial processes and community composition in the rhizosphere of European beech – The influence of plant C exudates Koranda, Marianne; Schnecker, Jörg; Kaiser, Christina Soil Biology and Biochemistry, Vol. 43, Issue 3 https://doi.org/10.1016/j.soilbio.2010.11.022	journal	March 2011
Rhizosphere priming effects on soil carbon and nitrogen mineralization Zhu, Biao; Gutknecht, Jessica L. M.; Herman, Donald J. Soil Biology and Biochemistry, Vol. 76 https://doi.org/10.1016/j.soilbio.2014.04.033	journal	September 2014
Enzyme properties down the soil profile - A matter of substrate quality in rhizosphere and detritusphere Loeppmann, Sebastian; Blagodatskaya, Evgenia; Pausch, Johanna Soil Biology and Biochemistry, Vol. 103 https://doi.org/10.1016/j.soilbio.2016.08.023	journal	December 2016
Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools Meier, Ina C.; Finzi, Adrien C.; Phillips, Richard P. Soil Biology and Biochemistry, Vol. 106 https://doi.org/10.1016/j.soilbio.2016.12.004	journal	March 2017
Decoupling of priming and microbial N mining during a short-term soil incubation Wild, Birgit; Li, Jian; Pihlblad, Johanna Soil Biology and Biochemistry, Vol. 129 https://doi.org/10.1016/j.soilbio.2018.11.014	journal	February 2019
Wide-spread limitation of soil organic nitrogen transformations by substrate availability and not by extracellular enzyme content Noll, Lisa; Zhang, Shasha; Zheng, Qing Soil Biology and Biochemistry, Vol. 133 https://doi.org/10.1016/j.soilbio.2019.02.016	journal	June 2019
Contribution of different catalytic types of peptidases to soil proteolytic activity Nguyen, Trang; Kleber, Markus; Myrold, David D. Soil Biology and Biochemistry, Vol. 138 https://doi.org/10.1016/j.soilbio.2019.107578	journal	November 2019
What are the products of enzymatic cleavage of organic N? Warren, Charles Soil Biology and Biochemistry, Vol. 154 https://doi.org/10.1016/j.soilbio.2021.108152	journal	March 2021
Synthesis of methods used to assess soil protease activity Greenfield, Lucy M.; Puissant, Jérémy; Jones, Davey L. Soil Biology and Biochemistry, Vol. 158 https://doi.org/10.1016/j.soilbio.2021.108277	journal	July 2021
Effects of PGPR microbial inoculants on the growth and soil properties of Avena sativa, Medicago sativa, and Cucumis sativus seedlings Li, Haiyun; Qiu, Yizhi; Yao, Tuo Soil and Tillage Research, Vol. 199 https://doi.org/10.1016/j.still.2020.104577	journal	May 2020
Selective progressive response of soil microbial community to wild oat roots DeAngelis, Kristen M.; Brodie, Eoin L.; DeSantis, Todd Z. The ISME Journal, Vol. 3, Issue 2 https://doi.org/10.1038/ismej.2008.103	journal	November 2008
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
The elemental composition of virus particles: implications for marine biogeochemical cycles Jover, Luis F.; Effler, T. Chad; Buchan, Alison Nature Reviews Microbiology, Vol. 12, Issue 7 https://doi.org/10.1038/nrmicro3289	journal	June 2014
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 2020
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
A complete domain-to-species taxonomy for Bacteria and Archaea Parks, Donovan H.; Chuvochina, Maria; Chaumeil, Pierre-Alain Nature Biotechnology https://doi.org/10.1038/s41587-020-0501-8	journal	April 2020
Selection of micro-organisms in a spatially explicit environment and implications for plant access to nitrogen Kinzig, Ann P.; Harte, John Journal of Ecology, Vol. 86, Issue 5 https://doi.org/10.1046/j.1365-2745.1998.8650841.x	journal	October 1998
Global-level population genomics reveals differential effects of geography and phylogeny on horizontal gene transfer in soil bacteria Greenlon, Alex; Chang, Peter L.; Damtew, Zehara Mohammed Proceedings of the National Academy of Sciences, Vol. 116, Issue 30 https://doi.org/10.1073/pnas.1900056116	journal	July 2019
Mutualism and Competition between Plants and Decomposers: Implications for Nutrient Allocation in Ecosystems Harte, John; Kinzig, Ann P. The American Naturalist, Vol. 141, Issue 6 https://doi.org/10.1086/285511	journal	June 1993
CD-HIT Suite: a web server for clustering and comparing biological sequences Huang, Ying; Niu, Beifang; Gao, Ying Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btq003	journal	January 2010
GToTree: a user-friendly workflow for phylogenomics Lee, Michael D. Bioinformatics, Vol. 35, Issue 20 https://doi.org/10.1093/bioinformatics/btz188	journal	March 2019
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors Rawlings, Neil D.; Barrett, Alan J.; Finn, Robert Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1118	journal	November 2015
The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads Liao, Yang; Smyth, Gordon K.; Shi, Wei Nucleic Acids Research, Vol. 47, Issue 8 https://doi.org/10.1093/nar/gkz114	journal	February 2019
A plant perspective on nitrogen cycling in the rhizosphere Moreau, Delphine; Bardgett, Richard D.; Finlay, Roger D. Functional Ecology, Vol. 33, Issue 4 https://doi.org/10.1111/1365-2435.13303	journal	March 2019
Linkage between microbial functional genes and net N mineralisation in forest soils along an elevational gradient Wang, Jieying; He, Liyuan; Xu, Xiaofeng European Journal of Soil Science, Vol. 73, Issue 4 https://doi.org/10.1111/ejss.13276	journal	July 2022
Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition: RPE ENHANCES Q10 OF SOM DECOMPOSITION Zhu, Biao; Cheng, Weixin Global Change Biology, Vol. 17, Issue 6 https://doi.org/10.1111/j.1365-2486.2010.02354.x	journal	November 2010
The rhizosphere as a reservoir for opportunistic human pathogenic bacteria Berg, Gabriele; Eberl, Leo; Hartmann, Anton Environmental Microbiology, Vol. 7, Issue 11 https://doi.org/10.1111/j.1462-2920.2005.00891.x	journal	November 2005
Bacterial quorum sensing and nitrogen cycling in rhizosphere soil: Bacterial QS and rhizosphere nitrogen cycling DeAngelis, Kristen M.; Lindow, Steven E.; Firestone, Mary K. FEMS Microbiology Ecology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00550.x	journal	November 2008
Plant–microbe competition: does injection of isotopes of C and N into the rhizosphere effectively characterise plant use of soil N? Hill, Paul W.; Jones, Davey L. New Phytologist, Vol. 221, Issue 2 https://doi.org/10.1111/nph.15433	journal	September 2018
Short-Term Nitrogen Fertilization Affects Microbial Community Composition and Nitrogen Mineralization Functions in an Agricultural Soil Ouyang, Yang; Norton, Jeanette M. Applied and Environmental Microbiology, Vol. 86, Issue 5 https://doi.org/10.1128/AEM.02278-19	journal	December 2019
Mapping of Sugar and Amino Acid Availability in Soil around Roots with Bacterial Sensors of Sucrose and Tryptophan Jaeger, C. H.; Lindow, S. E.; Miller, W. Applied and Environmental Microbiology, Vol. 65, Issue 6 https://doi.org/10.1128/AEM.65.6.2685-2690.1999	journal	January 1999
Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5488-5491.2000	journal	December 2000
The Functional Significance of Bacterial Predators Hungate, Bruce A.; Marks, Jane C.; Power, Mary E. mBio, Vol. 12, Issue 2 https://doi.org/10.1128/mBio.00466-21	journal	April 2021
Successional Trajectories of Rhizosphere Bacterial Communities over Consecutive Seasons Shi, Shengjing; Nuccio, Erin; Herman, Donald J. mBio, Vol. 6, Issue 4 https://doi.org/10.1128/mBio.00746-15	journal	August 2015
Interaction Networks Are Driven by Community-Responsive Phenotypes in a Chitin-Degrading Consortium of Soil Microbes McClure, Ryan; Farris, Yuliya; Danczak, Robert mSystems, Vol. 7, Issue 5 https://doi.org/10.1128/msystems.00372-22	journal	October 2022
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon Starr, Evan P.; Shi, Shengjing; Blazewicz, Steven J. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0499-z	journal	July 2018
Nitrogen Mineralization: Challenges of a Changing Paradigm Schimel, Joshua P.; Bennett, Jennifer Ecology, Vol. 85, Issue 3 https://doi.org/10.1890/03-8002	journal	March 2004
Microbial Nitrogen Limitation Increases Decomposition Craine, Joseph M.; Morrow, Carl; Fierer, Noah Ecology, Vol. 88, Issue 8 https://doi.org/10.1890/06-1847.1	journal	August 2007
Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils Brzostek, Edward R.; Finzi, Adrien C. Ecology, Vol. 92, Issue 4 https://doi.org/10.1890/10-1803.1	journal	April 2011
Root Influence on Nitrogen Mineralization and Nitrification in Rhizosphere Soil Herman, D. J.; Johnson, K. K.; Jaeger, C. H. Soil Science Society of America Journal, Vol. 70, Issue 5 https://doi.org/10.2136/sssaj2005.0113	journal	January 2006
Rhizosphere priming: a nutrient perspective Dijkstra, Feike A.; Carrillo, Yolima; Pendall, Elise Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00216	journal	January 2013
Distributions of Extracellular Peptidases Across Prokaryotic Genomes Reflect Phylogeny and Habitat Nguyen, Trang T. H.; Myrold, David D.; Mueller, Ryan S. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00413	journal	March 2019
Revisiting Plant–Microbe Interactions and Microbial Consortia Application for Enhancing Sustainable Agriculture: A Review Vishwakarma, Kanchan; Kumar, Nitin; Shandilya, Chitrakshi Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.560406	journal	December 2020
Effect of Corn Steep Liquor (CSL) and Cassava Wastewater (CW) on Chitin and Chitosan Production by Cunninghamella elegans and Their Physicochemical Characteristics and Cytotoxicity Berger, Lúcia; Stamford, Thayza; Stamford-Arnaud, Thatiana Molecules, Vol. 19, Issue 3 https://doi.org/10.3390/molecules19032771	journal	February 2014
Effects of stoichiometry and temperature perturbations on beech leaf litter decomposition, enzyme activities and protein expression Keiblinger, K. M.; Schneider, T.; Roschitzki, B. Biogeosciences, Vol. 9, Issue 11 https://doi.org/10.5194/bg-9-4537-2012	journal	January 2012

Similar Records

Niche differentiation is spatially and temporally regulated in the rhizosphere

Journal Article · 2020 · The ISME Journal · OSTI ID:2281290

Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas; +8 more

Rhizosphere and detritusphere habitats modulate expression of soil N-cycling genes during plant development

Journal Article · 2023 · mSystems · OSTI ID:2203352

Sieradzki, Ella T.; Nuccio, Erin E.; Pett-Ridge, Jennifer; +1 more

Metatranscriptomics sheds light on the links between the functional traits of fungal guilds and ecological processes in forest soil ecosystems

Journal Article · 2023 · New Phytologist · OSTI ID:2473667

Auer, Lucas; Buée, Marc; Fauchery, Laure; +24 more

Title: Expression of macromolecular organic nitrogen degrading enzymes identifies potential mediators of soil organic N availability to an annual grass

Citation Formats

References (73)

Similar Records

Related Subjects