Dynamic Change in Enzyme Activity and Bacterial Community with long-term rice Cultivation in Mudflats

  • Yang Zhang
  • Qing Li
  • Yinglong Chen
  • Qigen DaiEmail author
  • Jian HuEmail author


Bacteria play an important role in the reclamation of mudflats. However, little is known about the effects of long-term rice cultivation on bacterial communities in mudflats. In this study, the bacterial community in mudflats with long-term rice cultivation was evaluated using Illumina MiSeq sequencing of the bacterial 16S rRNA genes. We found that the soil enzyme activity in mudflat soil demonstrated an overall increasing trend with an increase in rice planting years, while polyphenol oxidase activity decreased. There were significant differences in the microbial community composition between mudflat and paddy soil. There were high proportions of Proteobacteria and Bacteroidetes in mudflat soil, while the predominant phyla in paddy soil were Proteobacteria, Chloroflexi, and Acidobacteria. The dominant taxa were significantly correlated with electrical conductivity, organic matter, and total nitrogen. In addition, the proportion of Fe- and S-related bacteria in paddy soil was much higher than that of mudflat soil, including Anaeromyxobacter, Geobacter, Thiobacillus, Clostridium, and GOUTA19. Furthermore, the proportion of some nitrogen cycle-related bacteria (e.g., Nitrospira, Steroidobacter, Rhodoplanes) and some carbohydrate-degrading bacteria (e.g., Anaerolinea, Candidatus Solibacter) also increased with long-term rice cultivation in mudflat soil. These key microbial players are involved in the biogeochemical C, N, S, and Fe cycles of mudflat paddy soil during mudflat reclamation by rice cultivation. In short, the orderly succession of the bacterial community changed with the change of soil physical–chemical properties during long-term rice cultivation. In addition, key microbial players have a beneficial ecological function in enhancing soil fertility.



This research was supported by the National Science and Technology Support Project of China (2015BAD01B03), the Key Research and Development Plan of Jiangsu Province (BE2015337), and a Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Compliance with Ethical Standards

Conflict of interest

No potential conflict of interest was reported by the authors.

Supplementary material

284_2019_1636_MOESM1_ESM.doc (43 kb)
Supplementary material 1 (DOC 43 KB)


  1. 1.
    Long XH, Liu LP, Shao TY, Shao HB, Liu ZP (2016) Developing and sustainably utilize the coastal mudflat areas in China. Sci Total Environ 569–570:1077–1086CrossRefGoogle Scholar
  2. 2.
    Chen H, Xiao S, Cheng Y, Wang M (2000) Study of the exploitation and utilization of the yellow river delta tidal flat resources. Coast EngGoogle Scholar
  3. 3.
    Chi CM, Zhao CW, Sun XJ, Wang ZC (2012) Reclamation of saline-sodic soil properties and improvement of rice (oriza sativa L.) growth and yield using desulfurized gypsum in the west of songnen plain, northeast china. Geoderma 187-188:24–30 sCrossRefGoogle Scholar
  4. 4.
    Miao L, Liang ZW, Fu Y, Ma HY, Hang LH, Wang MM (2010) Impacts of sand amendment on rice (Oryza sativa L.) growth and yield in saline-sodic soils of North-East China. J Food Agric Environ 8(2):789–798Google Scholar
  5. 5.
    Van Horn DJ, Okie JG, Buelow HN, Gooseff MN, Barrett JE, Takacs-Vesbach CD (2014) Soil microbial responses to increased moisture and organic resources along a salinity gradient in a polar desert. Appl Environ Microbiol 80(10):3034–3043CrossRefGoogle Scholar
  6. 6.
    Canfora L, Bacci G, Pinzari F, Papa GL, Dazzi C, Benedetti A (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a salineSoil? PLoS ONE 9(9):e106662CrossRefGoogle Scholar
  7. 7.
    Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens, NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem 66(5):1–9CrossRefGoogle Scholar
  8. 8.
    Wu YP, Zhang Y, Bi YM, Sun ZJ (2015) Biodiversity in saline and non-saline soils along the bohai sea coast, China Pedosphere 25(2):307–315CrossRefGoogle Scholar
  9. 9.
    Brussaard L, Ruiter PCD, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agric Ecosystems Environ 121(3):233–244CrossRefGoogle Scholar
  10. 10.
    Morrissey EM, Gillespie JL, Morina JC, Franklin RB (2014) Salinity affects microbial activity and soil organic matter content in tidal wetlands. Glob Change Biol 20(4):1351–1362CrossRefGoogle Scholar
  11. 11.
    Ikenaga M, Guevara R, Dean AL, Pisani C, Boyer JN (2010) Changes in community structure of sediment bacteria along the Florida coastal Everglades marsh-mangrove-seagrass salinity gradient. Microb Ecol 59(2):284–295CrossRefGoogle Scholar
  12. 12.
    Mu P, Jia H, Wang Q (2017) The effect of land use on bacterial communities in saline-alkali soil. Curr Microbiol 74(3):325–333CrossRefGoogle Scholar
  13. 13.
    Lin XG (2008) Principles and methods of soil microbiology research. Higher Education Press, BeijingGoogle Scholar
  14. 14.
    Wang P, Liu YL, Li QL, Cheng K, Zheng JF, Zhang XH, Zheng JW, Joseph S, Pan GX (2015) Long-term rice cultivation stabilizes soil organic carbon and promotes soil microbial activity in a salt marsh derived soil chronosequence. Sci Rep 5(8):15704CrossRefGoogle Scholar
  15. 15.
    Liu C, Xu JM, Ding NF, Fu Q, Guo B, Lin Y, Li H, Li N (2013) The effect of long-term reclamation on enzyme activities and microbial community structure of saline soil at Shangyu, China. Environ Earth Sci 69(1):151–159CrossRefGoogle Scholar
  16. 16.
    Guénon R, Vennetier M, Dupuy N, Roussos S, Pailler A, Gros R (2013) Trends in recovery of mediterranean soil chemical properties and microbial activities after infrequent and frequent wildfires. Land Degrad Dev 24(2):115–128CrossRefGoogle Scholar
  17. 17.
    Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store. Nature 409(6817):149CrossRefGoogle Scholar
  18. 18.
    Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 359(6373):320–325CrossRefGoogle Scholar
  19. 19.
    Sato K, Kato Y, Taguchi G, Masahiroet N, Akira A, Makoto S (2009) Chitiniphilus shinanonensis gen. nov. sp. nov. a novel chitin-degrading bacterium belonging to Betaproteobacteria. J Gen Appl Microbiol 55(2):147–153CrossRefGoogle Scholar
  20. 20.
    Rocker D, Brinkhoff T, Gruner N, Dogs M, Simon M (2012) Composition of humic acid-degrading estuarine and marinebacterial communities. FEMS Microbiol Ecol 80(1):45–63CrossRefGoogle Scholar
  21. 21.
    Liu C, Ding N, Fu Q, Brookes PC, Xu JM, Guo B, Lin YC, Li H, Li NY (2016) The influence of soil properties on the size and structure of bacterial and fungal communities along a paddy soil chronosequence. Eur J Soil Biol 76:9–18CrossRefGoogle Scholar
  22. 22.
    Sekiguchi Y, Yamada T, Hanada S, Ohashi A, Harada H, Kamagata Y (2003) Anaerolinea thermophila gen.nov.sp.nov. and caldilinea aerophila gen. nov. sp. nov. novel filamentous thermophiles that represent a previously uncultured lineage of the domain bacteria at the subphylum level. Int J Syst Evol Microbiol 53(6):1843–1851CrossRefGoogle Scholar
  23. 23.
    Fang H, Liang D, Zhang T, Liu Y (2006) Anaerobic treatment of phenol in wastewater under thermophilic condition. Water Res 40:427–434CrossRefGoogle Scholar
  24. 24.
    Dorador C, Meneses D, Urtuvia V, Demergasso C, Vila I, Witzel K-P, Imhoff JF (2009) Diversity of Bacteroidetes in high-altitude saline evaporitic basins in northern Chile. J Geophys Res Biogeosci 114(G2):65CrossRefGoogle Scholar
  25. 25.
    Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9(6):403–413CrossRefGoogle Scholar
  26. 26.
    Timonen S, Sinkko H, Sun H, Sietiö OM, Rintakanto JM, Kiheri H, Heinonsalo J (2017) Ericoid roots and mycospheres govern plant-specific bacterial communities in boreal forest humus. Microb Ecol 73(4):1–15CrossRefGoogle Scholar
  27. 27.
    Steppe TF, Olson JB, Paerl HW, Litaker RW, Belnap J (1996) Consortial N2-fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol Ecol 21(3):149–156CrossRefGoogle Scholar
  28. 28.
    Li K, Liu R, Zhang H, Yun J (2013) The diversity and abundance of bacteria and oxygenic phototrophs in saline biological desert crusts in Xinjiang, Northwest China. Microb Ecol 66(1):40–48CrossRefGoogle Scholar
  29. 29.
    Lopes AR, Manaia CM, Nunes OC (2014) Bacterial community variations in an alfalfa-rice rotation system revealed by 16S rRNA gene 454-pyrosequencing. FEMS Microbiol Ecol 87(3):650–663CrossRefGoogle Scholar
  30. 30.
    Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJP, Gorby YA, Goodwin S (1993) Geobacter metallireducens gen. nov. sp. nov. a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159(4):336–344CrossRefGoogle Scholar
  31. 31.
    Tuovinen OH, Kelly DP (1974) Studies on the growth of Thiobacillus ferrooxidans. Arch Microbiol 95(1):165–180CrossRefGoogle Scholar
  32. 32.
    Akagi J, Campbell LL (1962) Studies on thermophilic sulfate-reducing bacteria III. Adenosine triphosphate-sulfurylase of Clostridium nigrificans and Desulfovibrio desulfuricans. J Bacteriol 84(6):1194–1201Google Scholar
  33. 33.
    He Q, Sanford RA (2003) Characterization of Fe(iii) reduction by chlororespiring Anaeromyxobacter dehalogenans. Appl Environ Microbiol 69(5):2712–2718CrossRefGoogle Scholar
  34. 34.
    Davidson EA, Chorover J, Dail DB (2003) A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis. Glob Change Biol 9(2):228–236CrossRefGoogle Scholar
  35. 35.
    Pester M, Maixner F, Berry D, Rattei T, Koch H, Lücker S, Nowka B, Richter A, Spieck E, Lebedeva E (2014) NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing N itrospira. Environ Microbiol 16(10):3055–3071CrossRefGoogle Scholar
  36. 36.
    Wang PH, Leu YL, Ismail W, Tang SL, Tsai CY, Chen HJ, Kao AT, Chiang YR (2013) Anaerobic and aerobic cleavage of the steroid core ring structure by steroidobacter denitrificans. J Lipid Res 54(5):1493–1504CrossRefGoogle Scholar
  37. 37.
    Rime T, Hartmann M, Brunner I, Widmer F, Zeyer J, Frey B (2015) Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol Ecol 24(5):1091CrossRefGoogle Scholar
  38. 38.
    Harada N, Nishiyama M, Otsuka S, Matsumoto S (2005) Effects of inoculation of phototrophic purple bacteria on grain yield of rice and nitrogenase activity of paddy soil in a pot experiment. Soil Sci Plant Nutr 51(3):361–367CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops/Research Institute of Rice Industry Engineering TechnologyYangzhou UniversityYangzhouChina
  2. 2.College of Environmental Science and EngineeringYangzhou UniversityYangzhouChina

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