Cited by 68Soil Carbon and Nitrogen DynamicsMicrobial Community Ecology and PhysiologyPlant-Microbe Interactions and Immunity

The DOI matches its Crossref record.

Fertilization shapes a well-organized community of bacterial decomposers for accelerated paddy straw degradation

Open access

Abstract

Straw, mainly dry stalks of crops, is an agricultural byproduct. Its incorporation to soils via microbial redistribution is an environment-friendly way to increase fertility. Fertilization influences soil microorganisms and straw degradation. However, our up to date knowledge on the responses of the straw decomposers to fertilization remains elusive. To this end, inoculated with paddy soils with 26-year applications of chemical fertilizers, organic amendments or controls without fertilization, microcosms were anoxically incubated with 13 C-labelled rice straw amendment. DNA-based stable isotope probing and molecular ecological network analysis were conducted to unravel how straw degrading bacterial species shift in responses to fertilizations, as well as evaluate what their roles/links in the microbiome are. It was found that only a small percentage of the community ecotypes was participating into straw degradation under both fertilizations. Fertilization, especially with organic amendments decreased the predominance of Firmicutes- and Acidobacteria-like straw decomposers but increased those of the copiotrophs, such as β-Proteobacteria and Bacteroidetes due to increased soil fertility. For the same reason, fertilization shifted the hub species towards those of high degrading potential and created a more stable and efficient microbial consortium. These findings indicate that fertilization shapes a well-organized community of decomposers for accelerated straw degradation.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-018-26375-8

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 75

  1. Dominguez-Escriba, L. & Porcar, M. Rice straw management: the big waste. Biofuel Bioprod. Bior. 4, 154–159 (2010). · DOI
  2. Liu, H., Jiang, G. M., Zhuang, H. Y. & Wang, K. J. Distribution, utilization structure and potential of biomass resources in rural China: With special references of crop residues. Renew Sust. Energ. Rev. 12, 1402–1418 (2008). · DOI
  3. Wang, Y. J., Bi, Y. Y. & Gao, C. Y. The assessment and utilization of straw resources in China. Agr. Sci. China 9, 1807–1815 (2010). · DOI
  4. McLaughlin, O., Mawhood, B., Jamieson, C. & Slade, R. Rice straw for bioenergy: the effectiveness of policymaking and implementation in Asia. In: 24th European Biomass Conference and Exhibition Amsterdam, The Netherlands (2016).
  5. Yan, Z. Y. et al. The effects of initial substrate concentration, C/N ratio, and temperature on solid-state anaerobic digestion from composting rice straw. Bioresource Technol. 177, 266–273 (2015). · DOI
  6. Watanabe, A., Katoh, K. & Kimura, M. Effect of rice straw application on CH4 emission from paddy fields. 2. Contribution of organic-constituents in rice straw. Soil Sci. Plant Nutr. 39, 707–712 (1993). · DOI
  7. Bugg, T. D. H., Ahmad, M., Hardiman, E. M. & Singh, R. The emerging role for bacteria in lignin degradation and bio-product formation. Curr. Opin. Biotech. 22, 394–400 (2011). · DOI
  8. Marschner, P., Umar, S. & Baumann, K. The microbial community composition changes rapidly in the early stages of decomposition of wheat residue. Soil Biol. Biochem. 43, 445–451 (2011). · DOI
  9. Fierer, N., Bradford, M. A. & Jackson, R. B. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364 (2007). · DOI
  10. Fan, F. L. et al. Probing potential microbial coupling of carbon and nitrogen cycling during decomposition of maize residue by 13C-DNA-SIP. Soil Biol. Biochem. 70, 12–21 (2014). · DOI
  11. Jimenez, D. J. et al. Characterization of three plant biomass-degrading microbial consortia by metagenomics- and metasecretomics-based approaches. Appl. Microbiol. Biot. 100, 10463–10477 (2016). · DOI
  12. Jimenez, D. J., Chaves-Moreno, D. & van Elsas, J.D. Unveiling the metabolic potential of two soil-derived microbial consortia selected on wheat straw. Sci. Rep. 5 (2015). · DOI
  13. Rui, J. P., Peng, J. J. & Lu, Y. H. Succession of bacterial populations during plant residue decomposition in rice field soil. Appl. Environ. Microb. 75, 4879–4886 (2009). · DOI
  14. Bernard, L. et al. Dynamics and identification of soil microbial populations actively assimilating carbon from 13C-labelled wheat residue as estimated by DNA- and RNA-SIP techniques. Environ. Microbiol. 9, 752–764 (2007). · DOI
  15. Glissmann, K. & Conrad, R. Fermentation pattern of methanogenic degradation of rice straw in anoxic paddy soil. FEMS Microbiol. Ecol. 31, 117–126 (2000). · DOI
  16. Glissmann, K., Weber, S. & Conrad, R. Localization of processes involved in methanogenic in degradation of rice straw in anoxic paddy soil. Environ. Microbiol. 3, 502–511 (2001). · DOI
  17. Glissmann, K. & Conrad, R. Saccharolytic activity and its role as a limiting step in methane formation during the anaerobic degradation of rice straw in rice paddy soil. Biol. Fert. Soils 35, 62–67 (2002). · DOI
  18. Murase, J., Matsui, Y., Katoh, M., Sugimoto, A. & Kimura, M. Incorporation of 13C-labeled rice-straw-derived carbon into microbial communities in submerged rice field soil and percolating water. Soil Biol. Biochem. 38, 3483–3491 (2006). · DOI
  19. Shrestha, M., Shrestha, P. M. & Conrad, R. Bacterial and archaeal communities involved in the in situ degradation of 13C-labelled straw in the rice rhizosphere. Environ. Microbiol. Rep. 3, 587–596 (2011). · DOI
  20. Lee, C. G., Watanabe, T. & Asakawa, S. Bacterial community incorporating carbon derived from plant residue in an anoxic non-rhizosphere soil estimated by DNA-SIP analysis. J. Soil Sediment 17, 1084–1091 (2017). · DOI
  21. Pariz, C. M. et al. Straw decomposition of nitrogen-fertilized grasses intercropped with irrigated maize in an integrated crop-livestock system. Rev. Bras. Cienc. Solo. 35, 2029–2037 (2011). · DOI
  22. Chen, R. R. et al. Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Global Change Biol. 20, 2356–2367 (2014). · DOI
  23. Reinertsen, S. A., Elliott, L. F., Cochran, V. L. & Campbell, G. S. Role of available carbon and nitrogen in determining the rate of wheat straw decomposition. Soil Biol. Biochem. 16, 459–464 (1984). · DOI
  24. Koranda, M. et al. Fungal and bacterial utilization of organic substrates depends on substrate complexity and N availability. FEMS Microbiol. Ecol. 87, 142–152 (2014). · DOI
  25. Eichorst, S. A. & Kuske, C. R. Identification of cellulose-responsive bacterial and fungal communities in geographically and edaphically different soils by using stable isotope probing. Appl. Environ. Microb. 78, 2316–2327 (2012). · DOI
  26. Barberan, A., Bates, S. T., Casamayor, E. O. & Fierer, N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 6, 343–351 (2012). · DOI · Paper page
  27. Deng, Y. et al. Molecular ecological network analyses. BMC Bioinformatics 13 (2012). · DOI
  28. Faust, K. & Raes, J. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538–550 (2012). · DOI
  29. Ling, N. et al. Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biol. Biochem. 99, 137–149 (2016). · DOI
  30. Feng, Y. Z. et al. Balanced fertilization decreases environmental filtering on soil bacterial community assemblage in north China. Front. Microbiol. 8 (2017). · DOI
  31. Wegner, C. E. & Liesack, W. Microbial community dynamics during the early stages of plant polymer breakdown in paddy soil. Environ. Microbiol. 18, 2825–2842 (2016). · DOI
  32. Semenov, A. V. et al. Impact of incorporated fresh 13C-potato tissues on the bacterial and fungal community composition of soil. Soil Biol. Biochem. 49, 88–95 (2012). · DOI
  33. Espana, M. et al. Identification of active bacteria involved in decomposition of complex maize and soybean residues in a tropical Vertisol using 15N-DNA stable isotope probing. Pedobiologia 54, 187–193 (2011). · DOI
  34. Zhou, Y. Z. et al. Omics-based interpretation of synergism in a soil-derived cellulose-degrading microbial community. Sci. Rep. 4 (2014). · DOI
  35. Weber, S., Stubner, S. & Conrad, R. Bacterial populations colonizing and degrading rice straw in anoxic paddy soil. Appl. Environ. Microb. 67, 1318–1327 (2001). · DOI
  36. Flint, H. J., Scott, K. P., Duncan, S. H., Louis, P. & Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3, 289–306 (2012). · DOI · Paper page
  37. DeAngelis, K. M. et al. Evidence supporting dissimilatory and assimilatory lignin degradation in Enterobacter lignolyticus SCF1. Front. Microbiol. 4 (2013). · DOI
  38. Kameshwar, A. K. S. & Qin, W. S. Recent developments in using advanced sequencing technologies for the genomic studies of lignin and cellulose degrading microorganisms. Int. J. Biol. Sci. 12, 156–171 (2016). · DOI
  39. Liesack, W., Schnell, S. & Revsbech, N. P. Microbiology of flooded rice paddies. FEMS Microbiol. Rev. 24, 625–645 (2000). · DOI
  40. Book, A.J. et al. Cellulolytic streptomyces strains associated with herbivorous insects share a phylogenetically linked capacity to degrade lignocellulose. Appl. Environ. Microb. 80, 4692–4701 (2014). · DOI
  41. Wirth, S. & Ulrich, A. Cellulose-degrading potentials and phylogenetic classification of carboxymethyl-cellulose decomposing bacteria isolated from soil. Syst. Appl. Microbiol. 25, 584–591 (2002). · DOI
  42. Taylor, C. R. et al. Isolation of bacterial strains able to metabolize lignin from screening of environmental samples. J. Appl. Microbiol. 113, 521–530 (2012). · DOI
  43. Garcia, R. & Müller, R. The Family Polyangiaceae. 247–279 (2014). · DOI
  44. Dumont, M. G., Pommerenke, B., Casper, P. & Conrad, R. DNA-, rRNA- and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment. Environ. Microbiol. 13, 1153–1167 (2011). · DOI
  45. Bowman, J. P., Sly, L. I., Hayward, A. C., Spiegel, Y. & Stackebrandt, E. Telluria-mixta (Pseudomonas-mixta Bowman, Sly, and Hayward 1988) gen-nov, comb-nov, and Telluria-chitinolytica sp-nov, soil-dwelling organisms which actively degrade polysaccharides. Int. J. Syst. Bacteriol. 43, 120–124 (1993). · DOI
  46. Xie, G. et al. Genome sequence of the cellulolytic gliding bacterium Cytophaga hutchinsonii. Appl. Environ. Microb. 73, 3536–3546 (2007). · DOI
  47. Hottes, A. K. et al. Transcriptional profiling of Caulobacter crescentus during growth on complex and minimal media. J. Bacteriol. 186, 1448–1461 (2004). · DOI
  48. Sheng, P. et al. Construction and Characterization of a Cellulolytic Consortium Enriched from the Hindgut of Holotrichia parallela Larvae. Int. J. Mol. Sci. 17 (2016). · DOI
  49. Seneviratne, G. Litter quality and nitrogen release in tropical agriculture: a synthesis. Biol. Fert. Soils 31, 60–64 (2000). · DOI
  50. Chen, H. H., Li, X. C., Hu, F. & Shi, W. Soil nitrous oxide emissions following crop residue addition: a meta-analysis. Global Change Biol. 19, 2956–2964 (2013). · DOI
  51. Albert, R., Jeong, H. & Barabasi, A. L. Error and attack tolerance of complex networks. Nature 406, 378–382 (2000). · DOI · Paper page
  52. Narisawa, N., Haruta, S., Arai, H., Ishii, M. & Igarashi, Y. Coexistence of antibiotic-producing and antibiotic-sensitive bacteria in biofilms is mediated by resistant bacteria. Appl. Environ. Microb. 74, 3887–3894 (2008). · DOI
  53. Wood, S. A. et al. Consequences of tropical forest conversion to oil palm on soil bacterial community and network structure. Soil Biol. Biochem. 112, 258–268 (2017). · DOI
  54. Latora, V. & Marchiori, M. Efficient behavior of small-world networks. Phys. Rev. Lett. 87 (2001). · DOI · Paper page
  55. West, D. B. Introduction to Graph Theory. Englewood Cliffs, NJ: Prentice Hall (1996).
  56. Giovannoni, S. J., Thrash, J. C. & Temperton, B. Implications of streamlining theory for microbial ecology. ISME J. 8, 1553–1565 (2014). · DOI
  57. Großkopf, T. & Soyer, O. S. Microbial diversity arising from thermodynamic constraints. ISME J. 10, 2725–2733 (2016). · DOI
  58. Zheng, S. X. et al. Soil microbial activity measured by microcalorimetry in response to long-term fertilization regimes and available phosphorous on heat evolution. Soil Biol. Biochem. 41, 2094–2099 (2009). · DOI
  59. Jing, Z. et al. Response and feedback of C mineralization to P availability driven by soil microorganisms. Soil Biol. Biochem. 105, 111–120 (2017). · DOI
  60. Dunne, J. A., Williams, R. J. & Martinez, N. D. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5, 558–567 (2002). · DOI
  61. Reichenbach, H., Lang, E., Schumann, P. & Sproer, C. Byssovorax cruenta gen. nov., sp nov., nom. rev., a cellulose-degrading myxobacterium: rediscovery of ‘Myxococcus cruentus’ Thaxter 1897. Int. J. Syst. Evol. Micr. 56, 2357–2363 (2006). · DOI
  62. Fontaine, S., Mariotti, A. & Abbadie, L. The priming effect of organic matter: a question of microbial competition? Soil Biol. Biochem. 35, 837–843 (2003). · DOI
  63. Bei, Q. C. et al. Heterotrophic and phototrophic 15N2 fixation and distribution of fixed 15N in a flooded rice-soil system. Soil. Biol. Biochem. 59, 25–31 (2013). · DOI
  64. Jia, Z. J. & Conrad, R. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11, 1658–1671 (2009). · DOI
  65. Neufeld, J. D., Dumont, M. G., Vohra, J. & Murrell, J. C. Methodological considerations for the use of stable isotope probing in microbial ecology. Microb. Ecol. 53, 435–442 (2007). · DOI
  66. Feng, Y. Z. et al. Bacillus asahii comes to the fore in organic manure fertilized alkaline soils. Soil Biol. Biochem. 81, 186–194 (2015). · DOI
  67. Magoc, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011). · DOI · Paper page
  68. Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013). · DOI
  69. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal 17, 10–12 (2011). · DOI · Paper page
  70. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microb. 73, 5261–5267 (2007). · DOI
  71. Zgadzaj, R. et al. Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. P. Natl. Acad. Sci. USA 113, E7996–E8005 (2016). · DOI
  72. Luo, F. et al. Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory. Bmc Bioinformatics 8 (2007). · DOI
  73. Olesen, J. M., Bascompte, J., Dupont, Y. L. & Jordano, P. The modularity of pollination networks. P. Natl. Acad. Sci. USA 104, 19891–19896 (2007). · DOI
  74. Anderson, M. J. & Walsh, D. C. I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol. Monogr. 83, 557–574 (2013). · DOI
  75. Lueders, T., Manefield, M. & Friedrich, M. W. Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ. Microbiol. 6, 73–78 (2004). · DOI

Cited by

Sorted by citations

Metadata

Authors
Zhan, Y., Liu, W., Bao, Y., Zhang, J., Petropoulos, E., Li, Z., Lin, X., & Feng, Y.
Affiliations
  • Chinese Academy of Sciences (CN)
  • Newcastle University (GB)
Corresponding author
Feng, Youzhi
Venue
Scientific Reports
Published
2018-05-22
Volume
8
Issue
1
Pages
7981-7981
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2804349277
Cited by
68
References
0
Citations by year
2026: 6 · 2025: 8 · 2024: 8 · 2023: 7 · 2022: 10 · 2021: 16 · 2020: 7 · 2019: 5 · 2018: 1
FWCI
6.78
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Newcastle University ePrints (Newcastle Univesity) (cc-by)
Funders
  • National Natural Science Foundation of China (41430859, 973 Program, 41671267, 2016YFD0200306)
  • Chinese Academy of Sciences (KFJ-STS-QYZD-020, XDB15020103, ISSASIP1639)
  • Youth Innovation Promotion Association of the Chinese Academy of Sciences (No. 2014271, 2016YFD0200306, 2014271)
  • Biotechnology and Biological Sciences Research Council (BB/K003240, BB/K003240/1)
  • National Key Research and Development Program of China (2016YFD0200306, 2014CB954500)
  • Youth Innovation Promotion Association
Topics
  • Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
Keywords
fertilization, soil microbial communities, organic amendments, mineral fertilizers, stable isotope probing, microbial ecological networks, hub species, copiotrophs, Firmicutes, Acidobacteria, Betaproteobacteria, Bacteroidetes, soil fertility, anaerobic incubation
MeSH terms
Agriculture, Biodegradation, Environmental, Fertilizers, Oryza, Soil, Soil Microbiology, Biomass, Crops, Agricultural, Microbial Consortia, Solid Waste, Microbiota

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review