Skip to main content
Log in

Identifying microbial drivers promoting plant growth on soil amended with composted aquatic plant: insight into nutrient transfer from aquatic to terrestrial systems

  • Special Feature: Original Article
  • Material transport and cycle in watersheds
  • Published:
Limnology Aims and scope Submit manuscript

Abstract

Effects of applying composted aquatic plants on soil chemistry, soil microbes (fungi and bacteria), and the growth of cultivated plant were demonstrated. To identify drivers promoting cultivated plant growth on soil amended with composted aquatic plant, empirical data of pot experiments were incorporated into structural equation models by hypothesizing causal relationships between the application of composted aquatic plants, soil chemistry, soil microbes, and cultivated plant growth. Cultivated plant growth, total carbon content, and bacterial and fungal richness in soil increased on soil applied with composted aquatic plants, and the composition of bacterial and fungal assemblages in soil were significantly different among the application treatments. Structural equation models explicitly demonstrated the relative importance of bacterial assemblages compared to soil chemistry as a promoter of cultivated plant growth in response to the application of composted aquatic plants. The present study is the first to demonstrate that the positive effects of composted aquatic plants on terrestrial plant growth are mediated by soil microbial processes. Our results could provide basic insights into the transfer and cycling of nutrients from aquatic to terrestrial systems through human activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Antunes LP, Martins LF, Pereira RV, Thomas AM, Barbosa D, Lemos LN, Silva GMM, Moura LMS, Epamino GWC, Digiampietri LA, Lombardi KC, Ramos PL, Quaggio RB, de Oliveira JCF, Pascon RC, da Cruz JB, da Silva AM, Setubal JC (2016) Microbial community structure and dynamics in thermophilic composting viewed through metagenomics and metatranscriptomics. Sci Rep 6:38915

    Article  CAS  Google Scholar 

  • Ban S, TodaT KM, Ishikawa K, Kohzu A, Imai A (2019) Modern lake ecosystem management by sustainable harvesting and effective utilization of aquatic macrophytes. Limnology 20:93–100

    Article  Google Scholar 

  • Browne MW, Cudeck R (1993) Alternative ways of assessing model fit. In: Bollen KA, Long JS (eds) Testing structural equation models. Sage Publications, Newbury Park, pp 136–162

    Google Scholar 

  • Chambers PA, Lacoul P, Murphy KJ, Thomaz SM (2008) Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595:9–26

    Article  Google Scholar 

  • Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547

    Article  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  Google Scholar 

  • Fujii S, Mori AS, Koide D, Makoto K, Matsuoka S, Osono T, Isbell F (2017) Disentangling relationships between plant diversity and decomposition processes under forest restoration. J Appl Ecol 54:80–90

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primer with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rust. Mol Ecol 2:113–118

    Article  CAS  Google Scholar 

  • Gratton C, Zanden MJV (2009) Productivity to land: comparison of lentic and lotic ecosystems. Ecology 90:2689–2699

    Article  Google Scholar 

  • Gunnarsson CC, Petersen CM (2007) Water hyacinths as a resource in agriculture and energy production: a literature review. Waste Manag 27:117–129

    Article  Google Scholar 

  • Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237

    Article  CAS  Google Scholar 

  • Hasegawa S (1939) Utilization and effect of aquatic plants at lakesides of Lake Biwa (in Japanese). Shiga Prefecture Agricultural Experiment Station, Shiga

    Google Scholar 

  • Hooper D, Coughlan J, Mullen M (2008) Structural equation modelling: guidelines for determining model fit. Electron J Bus Res Methods 6:53–60

    Google Scholar 

  • Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656–668

    Article  Google Scholar 

  • Lin Y, Ye G, Kuzyakov Y, Liu D, Fan J, Ding W (2019) Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol Biochem 134:187–196

    Article  CAS  Google Scholar 

  • Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120

    Article  Google Scholar 

  • Lori M, Symnaczik S, Mӓder P, De Deyn G, Gattinger A (2017) Organic farming enhance soil microbial abundance and activity—a meta-analysis and meta-regression. PLoS ONE 12:e0180442

    Article  Google Scholar 

  • Martínez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319

    Article  Google Scholar 

  • Matsuoka S, Mori AS, Kawaguchi E, Hobara S, Osono T (2016a) Disentangling the relative importance of host tree community, abiotic environment, and spatial factors on ectomycorrhizal fungal assemblages along an elevation gradient. FEMS Microb Ecol 92:fiw044

    Article  Google Scholar 

  • Matsuoka S, Kawaguchi E, Osono T (2016b) Temporal distance decay of similarity of ectomycorrhizal fungal community composition in a subtropical evergreen forest in Japan. FEMS Microb Ecol 92:fiw061

    Article  Google Scholar 

  • Ohtsuka T, Kuwabara Y, Haga H (2004) Estimated distribution and biomass of a submerged macrophyte community in Lake Biwa’s South Basin using an echo-sounder (in Japanese with English abstract). Jpn J Limnol 65:13–20

    Article  Google Scholar 

  • Osono T (2014) Metagenomic approach growths insights into fungal diversity and functioning. In: Sota T, Kagata H, Ando Y, Utsumi S, Osono T (eds) Species diversity and community structure. Springer, Berlin, pp 1–23

    Google Scholar 

  • Osono T, Takeda H (2004) Potassium, calcium, and magnesium dynamics during litter decomposition in a cool temperate forest. J For Res 9:23–31

    Article  CAS  Google Scholar 

  • Schindler DE, Smits AP (2017) Subsidies of aquatic resources in terrestrial ecosystems. Ecosystems 20:78–93

    Article  Google Scholar 

  • Tanabe AS (2016) Claident pipeline v0.2.2016.07.05, software distributed by the author at https://www.fifthdimension.jp/. Accessed 21 June 2019

  • Tanabe AS, Toju H (2013) Two new computational methods for universal DNA barcoding: a benchmark using barcode sequences of bacteria, archaea, animals, fungi, and land plants. PLoS ONE 8:e76910

    Article  CAS  Google Scholar 

  • Truog E (1930) The determination of the readily available phosphorus of soils. J Am Soc Agro 22:874–882

    Article  CAS  Google Scholar 

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Yabuzaki I, Kaneko M, Osono T, Hobara S (2014) Effects of composting years on chemical properties of waterweed compost and growth of Japanese mustard spinach (in Japanese with Engilsh abstract). J Rakuno Gakuen Univ 39:87–92

    Google Scholar 

  • Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. N. Okuda, Dr. Y. Sakai, Dr. S. Asano, Dr. I. Tayasu, Dr. S. Yachi, Dr. K. Wakita, Dr. T. Iwata, and Dr. S. Ban for useful comments and suggestions on experimental design, data analyses, and interpretations; Dr. S. Fujinaga and members of Center for Ecological Research, Kyoto University for assistance in laboratory works and pot experiments; staffs of Lake Biwa Policy Division of Shiga Prefecture and Ohmi Environment Conservation Foundation for providing composted aquatic plants and soil used in the pot experiments; Dr. H. Doi for critical comments on the manuscript; and Dr. E. Nakajima for critical reading of the manuscript. This study received partial financial support from Research Project (D06-14200119) of the Research Institute for Humanity and Nature (RIHN), Ohmi Environment Conservation Foundation, and from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) (No. 17K15199 and 18K05731).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shunsuke Matsuoka.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Ichiro Tayasu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 224 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsuoka, S., Kobayashi, Y., Hobara, S. et al. Identifying microbial drivers promoting plant growth on soil amended with composted aquatic plant: insight into nutrient transfer from aquatic to terrestrial systems. Limnology 21, 443–452 (2020). https://doi.org/10.1007/s10201-020-00613-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10201-020-00613-3

Keywords

Navigation