Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Responses of Soil Bacterial and Fungal Communities to Organic and Conventional Farming Systems in East China

  • Zhang, Hanlin (Eco-environmental Protection Institute, Shanghai Academy of Agricultural Science) ;
  • Zheng, Xianqing (Eco-environmental Protection Institute, Shanghai Academy of Agricultural Science) ;
  • Bai, Naling (Eco-environmental Protection Institute, Shanghai Academy of Agricultural Science) ;
  • Li, Shuangxi (Eco-environmental Protection Institute, Shanghai Academy of Agricultural Science) ;
  • Zhang, Juanqin (Eco-environmental Protection Institute, Shanghai Academy of Agricultural Science) ;
  • Lv, Weiguang (Eco-environmental Protection Institute, Shanghai Academy of Agricultural Science)
  • Received : 2018.09.06
  • Accepted : 2019.01.31
  • Published : 2019.03.28
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Abstract

Organic farming is considered an effective form of sustainable agricultural management. However, understanding of soil microbial diversity and composition under long-term organic and conventional farming is still limited and controversial. In this study, the Illumina MiSeq platform was applied to investigate the responses of soil bacterial and fungal diversity and compositions to organic farming (OF) and improved conventional farming (CF, applied straw retention) in the rice-wheat rotation system. The results highlighted that the alpha diversity of microbial communities did not differ significantly, except for higher bacterial diversity under OF. However, there were significant differences in the compositions of the soil bacterial and fungal communities between organic and conventional farming. Under our experimental conditions, through the ecological functional analysis of significant different or unique bacterial and fungal taxonomic members at the phyla and genus level, OF enhanced nitrogen, sulfur, phosphorus and carbon dynamic cycling in soil with the presence of Nodosilinea, Nitrospira, LCP-6, HB118, Lyngbya, GOUTA19, Mesorhizobium, Sandaracinobacter, Syntrophobacter and Sphingosinicella, and has the potential to strengthen soil metabolic ability with Novosphingobium. On the other hand, CF increased the intensity of nitrogen cycling with Ardenscatena, KD1-23, Iamia, Nitrosovibrio and Devosia, but enriched several pathogen fungal members, including Coniochaeta, Corallomycetella, Cyclaneusma, Cystostereum, Fistulina, Curvularia and Dissoconium.

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References

  1. Wakelin SA, Barratt BIP, Gerard E, Gregg AL, Brodie EL, Andersen GL, et al. 2013. Shifts in the phylogenetic structure and functional capacity of soil microbial communities follow alteration of native tussock grassland ecosystems. Soil. Biol. Biochem. 57: 675-682. https://doi.org/10.1016/j.soilbio.2012.07.003
  2. He JZ, Ge Y, Xu Z, Chen C. 2009. Linking soil bacterial diversity to ecosystem multifunctionality using backward elimination boosted trees analysis. J. Soil. Sediment. 9: 547-554. https://doi.org/10.1007/s11368-009-0120-y
  3. Hollister EB, Schadt CW, Palumbo AV, Ansley RJ, Boutton TW. 2010. Structural and functional diversity of soil bacterial and fungal communities following woody plant encroachment in the southern Great Plains. Soil. Biol. Biochem. 42: 1816-1824. https://doi.org/10.1016/j.soilbio.2010.06.022
  4. Silva MCPE, Semenov AV, Schmitt H, Elsas JDV, Salles JF. 2013. Microbemediated processes as indicators to establish the normal operating range of soil functioning. Soil. Biol. Biochem. 57: 995-1002. https://doi.org/10.1016/j.soilbio.2012.10.002
  5. Gomiero T, Pimentel D, Paoletti MG. 2011. Environmental impact of different agricultural management practices: conventional vs. organic agriculture. Crit. Rev. Plant Sci. 30: 95-124. https://doi.org/10.1080/07352689.2011.554355
  6. Luttikholt LWM. 2007. Principles of organic agriculture as formulated by the international federation of organic agriculture movements. Njas-Wagen. J. Life. Sci. 54: 347-360.
  7. Meng J, Li L, Liu H, Li Y, Li C, Wu G, et al. 2016. Biodiversity management of organic orchard enhances both ecological and economic profitability. PeerJ 4: e2137. https://doi.org/10.7717/peerj.2137
  8. Bell LW, Sparling B, Tenuta M, Entz MH. 2012. Soil profile carbon and nutrient stocks under long-term conventional and organic crop and Alfalfa-crop rotations and reestablished grassland. Agr. Ecosyst. Environ. 158: 156-163. https://doi.org/10.1016/j.agee.2012.06.006
  9. Senechkin IV, Speksnijder AGCL, Semenov AM, van Bruggen AHC, van Overbeek LS. 2010. Isolation and partial characterization of bacterial strains on low organic carbon medium from soils fertilized with different organic amendments. Microb. Ecol. 60: 829-839. https://doi.org/10.1007/s00248-010-9670-1
  10. Nelson DV, Sommers LE. 1982. Total carbon, organic carbon, and organic matter. pp.539-579. In: AL PageRH MillerDR Keeney. Methods of Soil Analysis. Chemical and microbiological properties. Agronomy no.9. Part 2, 2nd edn. ASA& SSSA, Madison, WI.
  11. Mehlich A. 1978. New extractant for soil test evaluation of phosphorus, potassium, magnesium, calcium, sodium, manganese and zinc 1. Commun. Soil. Sci. Plan. 9: 477-492. https://doi.org/10.1080/00103627809366824
  12. Zhou J, Wu L, Deng Y, Zhi X, Jiang YH, Tu Q, et al. 2011. Reproducibility and quantitation of amplicon sequencingbased detection. ISME J. 5: 1303-1313. https://doi.org/10.1038/ismej.2011.11
  13. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc. Natl. Acad. Sci. USA 109: 6241-6246. https://doi.org/10.1073/pnas.1117018109
  14. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software fordescribing and comparing microbial communities. Appl. Environ. Microb. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  15. Oksanen J, Kindt R, Legendre P, O'Hara B, Simpson GL, Solymos P, et al. 2008. The vegan package. Community ecology package. R package version 2.0-2
  16. Astier M, Merlin-Uribe Y, Villamil-Echeverri L, Garciarreal A, Gavito ME, Masera OR. 2014. Energy balance and greenhouse gas emissions in organic and conventional avocado orchards in Mexico. Ecol. Indic. 43: 281-287. https://doi.org/10.1016/j.ecolind.2014.03.002
  17. Syswerda S, Basso B, Hamilton S, Tausig J, Robertson G. 2012. Long-term nitrate loss along an agricultural intensity gradient in the Upper Midwest USA. Agr. Ecosyst. Environ. 149: 10-19. https://doi.org/10.1016/j.agee.2011.12.007
  18. Wang Q, Zhang J, Xin X, Zhao B, Ma D, Zhang H. 2016. The accumulation and transfer of arsenic and mercury in the soil under a long-term fertilization treatment. J. Soil. Sediments 16: 427-437. https://doi.org/10.1007/s11368-015-1227-y
  19. Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microb. 75: 5111-5120. https://doi.org/10.1128/AEM.00335-09
  20. Crowder DW, Northfield TD, Strand MR, Snyder WE. 2010. Organic agriculture promotes evenness and natural pest control. Nature 466: 109-112. https://doi.org/10.1038/nature09183
  21. Li R, Khafipour E, Krause DO, Entz MH, de Kievit DR, Fernando WGD. 2012. Pyrosequencing reveals the influence of organic and conventional farming systems on bacterial communities. PLoS One 7: e51897. https://doi.org/10.1371/journal.pone.0051897
  22. Wang W, Wang H, Feng Y, Wang L, Xiao X, Xi Y, et al. 2016. Consistent responses of the microbial community structure to organic farming along the middle and lower reaches of the Yangtze River. Sci. Rep. 6: 35046. https://doi.org/10.1038/srep35046
  23. Montes-Borrego M, Navas-Cortes JA, Landa BB. 2013. Linking microbial functional diversity of olive rhizosphere soil to management systems in commercial orchards in southern Spain. Agr. Ecosyst. Environ. 181: 169-178. https://doi.org/10.1016/j.agee.2013.09.021
  24. Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA. 2011. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front. Microbiol. 2: 94. https://doi.org/10.3389/fmicb.2011.00094
  25. Souza RC, Cantao ME, Vasconcelos ATR, Nogueira MA, Hungria M. 2013. Soil metagenomics reveals differences under conventional and notillage with crop rotation or succession. Appl. Soil. Ecol. 72: 49-61. https://doi.org/10.1016/j.apsoil.2013.05.021
  26. Nowka B, Daims H, Spieck E. 2015. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl. Environ. Microb. 81: 745-753. https://doi.org/10.1128/AEM.02734-14
  27. Li C, Tang L, Jia Z, Li Y. 2015. Profile changes in the soil microbial community when desert becomes oasis. PLoS One 10: e0139626. https://doi.org/10.1371/journal.pone.0139626
  28. Belen C, Nicolas R, Roberto A, Alejandro M, Martin PV. 2014. Structure, Composition and metagenomic profile of soil microbiomes associated to agricultural land use and tillage systems in argentine pampas. PLoS One 9: e99949. https://doi.org/10.1371/journal.pone.0099949
  29. Zhou G, Zhang J, Zhang C, Feng Y, Chen L, Yu Z, et al. 2016. Effects of changes in straw chemical properties and alkaline soils on bacterial communities engaged in straw decomposition at different temperatures. Sci. Rep. 6: 22186. https://doi.org/10.1038/srep22186
  30. Wang F, Liang Y, Jiang Y, Yang Y, Xue K, Xiong J, et al. 2015. Planting increases the abundance and structure complexity of soil core functional genes relevant to carbon and nitrogen cycling. Sci. Rep. 5: 14345. https://doi.org/10.1038/srep14345
  31. Ma A, Zhuang X, Wu J, Cui M, Lv D, Liu C, et al. 2013. Ascomycota members dominate fungal communities during straw residue decomposition in arable soil. PLoS One 8: e66146. https://doi.org/10.1371/journal.pone.0066146
  32. Richardson M. 2009. The ecology of the Zygomycetes and its impact on environmental exposure. Clin. Microbiol. Infect. 15: 2-9. https://doi.org/10.1111/j.1469-0691.2009.02972.x
  33. Antunes PM, Lehmann A, Hart MM, Baumecker M, Rillig MC. 2012. Long-term effects of soil nutrient deficiency on arbuscular mycorrhizal communities. Func. Ecol. 26: 532-540. https://doi.org/10.1111/j.1365-2435.2011.01953.x
  34. Martiny AC, Treseder K, Pusch G. 2013. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 7: 830-838. https://doi.org/10.1038/ismej.2012.160
  35. Kumar R, Verma H, Haider S, Bajaj A, Sood U, Ponnusamy K, et al. 2017. Comparative genomic analysis reveals habitatspecific genes and regulatory hubs within the genus novosphingobium. mSystems 2: e00020-17.
  36. Zhang Y, Wang C, He F, Liu B, Xu D, Xia S, et al. 2016. Insitu adsorption-biological combined technology treating sediment phosphorus in all fractions. Sci. Rep. 6: 29725. https://doi.org/10.1038/srep29725
  37. Mukherjee C, Chowdhury R, Ray K. 2015. Phosphorus recycling from an unexplored source by polyphosphate accumulating microalgae and cyanobacteria-A step to phosphorus security in agriculture. Front. Microbiol. 6: 1421.
  38. Sun M, Xiao T, Ning Z, Xiao E, Sun W. 2015. Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl. Microbiol. Biotechnol. 99: 2911-2922. https://doi.org/10.1007/s00253-014-6194-5
  39. Ghosh W, Roy P. 2006. Mesorhizobium thiogangeticum sp. nov. a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int. J. Syst. Evol. Microbiol. 56: 91-97. https://doi.org/10.1099/ijs.0.63967-0
  40. Gich F, Schubert K, Bruns A, Hoffelner H, Overmann J. 2005. Specific detection, isolation, and characterization of selected, previously uncultured members of the freshwater bacterioplankton community. Appl. Environ. Microbiol. 71: 5908-5919. https://doi.org/10.1128/AEM.71.10.5908-5919.2005
  41. Gan Y, Qiu Q, Liu P, Rui J, Lu Y. 2012. Syntrophic oxidation of propionate in rice field soil at 15 and $30^{\circ}C$ under methanogenic conditions. Appl. Environ. Microbiol. 78: 4923-4932. https://doi.org/10.1128/AEM.00688-12
  42. Hu J, Yang H, Long X, Liu Z, Rengel Z. 2016. Pepino (Solanum muricatum) planting increased diversity and abundance of bacterial communities in karst area. Sci. Rep. 6: 21938. https://doi.org/10.1038/srep21938
  43. Chaneva G, Furnadzhieva S, Minkova K, Lukavsky J. 2007. Effect of light and temperature on the cyanobacterium Arthronema africanum a prospective phycobiliprotein producing strain. J. Appl. Phycol. 19: 537-544. https://doi.org/10.1007/s10811-007-9167-6
  44. Puggioni V, Tempel S, Latifi A. 2016. Distribution of hydrogenases in cyanobacteria: a phylum-wide genomic survey. Front. Genet. 7: 223.
  45. Xia W, Zhang C, Zeng X, Feng Y, Weng J, Lin X, et al. 2011. Autotrophic growth of nitrifying community in an agricultural soil. ISME J. 5: 1226-1236. https://doi.org/10.1038/ismej.2011.5
  46. Zhang Y, Xu J, Riera N, Jin T, Li J, Wang N. 2017. Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome. Microbiome 5: 97. https://doi.org/10.1186/s40168-017-0304-4
  47. Kurahashi M, Fukunaga Y, Sakiyama Y, Harayama S, Yokota A. 2009. Iamia majanohamensis gen. nov., sp. nov., an actinobacterium isolated from sea cucumber Holothuria edulis, and proposal of Iamiaceae fam. nov. Int. J. Syst. Evol. Microbiol. 59: 869-873. https://doi.org/10.1099/ijs.0.005611-0
  48. Rivas R, Velazquez E, Willems A, Vizcaino N, Subba-Rao NS, Mateos PF, et al. 2002. A new species of devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume neptunia natans (L.f.) druce. Appl. Environ. Microbiol. 68: 5217-5222. https://doi.org/10.1128/AEM.68.11.5217-5222.2002
  49. Shah V, Shah S, Kambhampati MS, Ambrose J, Smith N, Dowd SE, et al. 2011. Bacterial and archaea community present in the pine barrens forest of long island, NY: unusually high percentage of ammonia oxidizing bacteria. PLoS One 6: e26263. https://doi.org/10.1371/journal.pone.0026263
  50. Skennerton CT, Ward LM, Michel A, Metcalfe K, Valiente C, Mullin S, et al. 2015. Genomic reconstruction of an uncultured hydrothermal vent gammaproteobacterial methanotroph (family methylothermaceae) indicates multiple adaptations to oxygen limitation. Front. Microbiol. 6: 1425. https://doi.org/10.3389/fmicb.2015.01425
  51. Fernandez H, Prandoni N, Fernandez-Pascual M, Fajardo S, Morcillo C, Diaz E, et al. 2014. Azoarcus sp. CIB, an anaerobic biodegrader of aromatic compounds shows an endophytic lifestyle. PLoS One 9: e110771. https://doi.org/10.1371/journal.pone.0110771
  52. McCormick SP, Price NPJ, Kurtzmana CP. 2012. Glucosylation and other biotransformations of T-2 toxin by yeasts of the trichomonascus clade. Appl. Environ. Microbiol. 78: 8694-8702. https://doi.org/10.1128/AEM.02391-12
  53. Lombard L, Crous PW. 2012. Phylogeny and taxonomy of the genus Gliocladiopsis. Persoonia 28: 25-33. https://doi.org/10.3767/003158512X635056
  54. Seven J, Polle A. 2014. Subcellular nutrient element localization and enrichment in ecto-and arbuscular mycorrhizas of field-grown beech and ash trees indicate functional differences. PLoS One 9: e114672. https://doi.org/10.1371/journal.pone.0114672
  55. Nakagawa T, Nagaoka T, Taniguchi S, Miyaji T, Tomizuka N. 2004. Isolation and characterization of psychrophilic yeasts producing cold-adapted pectinolytic enzymes. Lett. Appl. Microbiol. 38: 383-387. https://doi.org/10.1111/j.1472-765X.2004.01503.x
  56. Piśkiewicz AM, Duyts H, Berg MP, Costa SR. van der Putten WH. 2007. Soil microorganisms control plant ectoparasitic nematodes in natural coastal foredunes. Oecologia 152: 505-514. https://doi.org/10.1007/s00442-007-0678-2
  57. Gasoni L, de Gurfinkel BS. 1997. The endophyte Cladorrhinum forcundissimum in cotton roots: phosphorus uptake and host growth. Mycol. Res. 101: 867-870. https://doi.org/10.1017/S0953756296003462
  58. Torres-Cortes G, Ghignone S, Bonfante P, Schusslera A. 2015. Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasmafungus association. Proc. Natl. Acad. Sci. USA 112: 7785-7790. https://doi.org/10.1073/pnas.1501540112
  59. Damm U, Fourie PH, Crous PW. 2010. Coniochaeta (Lecythophora), Collophora gen. nov. and Phaeomoniella species associated with wood necroses of Prunus trees. Persoonia 24: 60-80. https://doi.org/10.3767/003158510X500705
  60. Floudasaf D, Heldb BW, Rileyc R, Nagyag LG, Koehlerd G, Ransdelld AS, et al. 2015. Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. Fungal Genet Biol. 76: 78-92. https://doi.org/10.1016/j.fgb.2015.02.002
  61. Ganley, R. J., Brunsfeld, S. J. & Newcombe, G. 2004. A community of unknown, endophytic fungi in western white pine. Proc. Nal. Acad. Sci. USA 101: 10107-10112. https://doi.org/10.1073/pnas.0401513101
  62. Jiang YL, Z hang TY. 2007. Notes on soild ematiaceous hyphomycetes. Mycosystema 26: 17-21. https://doi.org/10.3969/j.issn.1672-6472.2007.01.004
  63. Gleason ML, Batzer JC, Sun G, Zhang R, Arias MMD, Sutton TB, et al. 2011. A new view of sooty blotch and flyspeck. Plant. Dis. 95: 368-383. https://doi.org/10.1094/PDIS-08-10-0590

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