Skip to main content
Log in

Community structure, diversity, and species dominance of bacteria, fungi, and nematodes from naturally and conventionally farmed soil: a case study on Japanese apple orchards

  • Published:
Organic Agriculture Aims and scope Submit manuscript

Abstract

Although there has been much research on soil microbial communities in organic farming, little research has been reported on those in natural farming (no fertilizer use). Soil chemical properties and microbial and nematode communities in naturally (Orchard-N) and conventionally (Orchard-C) farmed apple orchards were compared over 3 years as a case study. The levels of nitrate nitrogen and available phosphate were significantly lower in Orchard-N than in Orchard-C. Bacterial evenness and nematode evenness and richness using denaturing gradient gel electrophoresis (DGGE) were higher in Orchard-N than in Orchard-C. All DGGE bands were identified by relative mobility values, termed relative front (Rf) values, and the Rf value of each band was classified into three dominant groups based on intensity: high, middle, and low intensities (HD, MD, and LD, respectively). Principal component analysis (PCA) on a correlation matrix showed that Orchard-N was characterized as MD/LD, corresponding to species of Alphaproteobacteria (bacteria), Actinobacteria (bacteria), Basidiomycota (fungi), Chaetomium (fungi), and Enoplea (nematodes). In contrast, Orchard-C was characterized by HD, corresponding to species of Gammaproteobacteria (bacteria), Fusarium (fungi), and Pratylenchus (nematodes), and MD/LD, similarly, Capnodiales (fungi) and Chloroflexi (bacteria). PCA on a variance–covariance matrix showed that annual changes in fungal and nematode community structures were larger in Orchard-C than in Orchard-N due to the large effect of HD. Quantitative polymerase chain reaction revealed that Orchard-N had higher bacterial and lower fungal abundance than Orchard-C. Based on these results, the relationship between the organism communities and the soil ecosystem in both orchards is discussed.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acosta-Martinez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770

    Article  CAS  Google Scholar 

  • Bissett A, Richardson A, Baker G, Thrall P (2011) Long-term land use effects on soil microbial community structure and function. Appl Soil Ecol 51:66–78

    Article  Google Scholar 

  • Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75

    Article  CAS  PubMed  Google Scholar 

  • Bongers T (1999) The maturity index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant Soil 212:13–22

    Article  CAS  Google Scholar 

  • Briar S, Grewal P, Somasekhar N, Stinner D, Miller S (2007) Soil nematode community, organic matter, microbial biomass and nitrogen dynamics in field plots transitioning from conventional to organic management. Appl Soil Ecol 37:256–266

    Article  Google Scholar 

  • Brussaard L, de Ruiter P, Brown G (2007) Soil biodiversity for agricultural sustainability. Agric Ecosyst Environ 121:233–244

    Article  Google Scholar 

  • Buchan D, Gebremikael M, Ameloot N, Sleutel S, De Neve S (2013) The effect of free-living nematodes on nitrogen mineralisation in undisturbed and disturbed soil cores. Soil Biol Biochem 60:142–155

    Article  CAS  Google Scholar 

  • Buee M, Reich M, Murat C, Morin E, Nilsson R, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    Article  CAS  PubMed  Google Scholar 

  • Bulluck L, Brosius M, Evanylo G, Ristaino J (2002) Organic and synthetic fertility amendments influence soil microbial, physical and chemical properties on organic and conventional farms. Appl Soil Ecol 19:147–160

    Article  Google Scholar 

  • Chapin F, Zavaleta E, Eviner V, Naylor R, Vitousek P, Reynolds H, Hooper D, Lavorel S, Sala O, Hobbie S, Mack M, Diaz S (2000) Consequences of changing biodiversity. Nature 405:234–242

    Article  CAS  PubMed  Google Scholar 

  • Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112

    Article  CAS  PubMed  Google Scholar 

  • Deruiter P, Vanveen J, Moore J, Brussaard L, Hunt H (1993) Calculation of nitrogen mineralization in soil food webs. Plant Soil 157:263–273

    Article  CAS  Google Scholar 

  • Ding G, Piceno Y, Heuer H, Weinert N, Dohrmann A, Carrillo A, Andersen G, Castellanos T, Tebbe C, Smalla K (2013) Changes of soil bacterial diversity as a consequence of agricultural land use in a semi-arid ecosystem. Plos One 8:e59497

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doran J, Sarrantonio M, Liebig M, Sparks D (1996) Soil health and sustainability. Adv Agron 56(56):1–54

    Article  CAS  Google Scholar 

  • Drinkwater LE, Letourneau DK, Workneh F, van Bruggen AHC, Shennan C (1995) Fundamental differences between conventional and organic tomato agroecosystems in California. Ecol Appl 5:1098–1112

    Article  Google Scholar 

  • Esperschuetz J, Gattinger A, Mader P, Schloter M, Fliessbach A (2007) Response of soil microbial biomass and community structures to conventional and organic farming systems under identical crop rotations. FEMS Microbiol Ecol 61:26–37

    Article  CAS  Google Scholar 

  • Ferris H, Bongers T, de Goede R (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29

    Article  Google Scholar 

  • Fierer N, Jackson J, Vilgalys R, Jackson R (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fierer N, Strickland M, Liptzin D, Bradford M, Cleveland C (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    Article  PubMed  Google Scholar 

  • Foucher A, Bongers T, Noble LR, Wilson MJ (2004) Assessment of nematode biodiversity using DGGE of 18S rDNA following extraction of nematodes from soil. Soil Biol Biochem 36:2027–2032

    Article  CAS  Google Scholar 

  • Fukuoka M (1978) The one straw revolution. New york review book, New York

    Google Scholar 

  • Girvan MS, Bullimore J, Ball AS, Pretty JN, Osborn AM (2004) Responses of active bacterial and fungal communities in soils under winter wheat to different fertilizer and pesticide regimens. Appl Environ Microbiol 70:2692–2701

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendonca-Hagler L, Smalla K (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 69:3758–3766

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He Y, Isono S, Shibuya M, Tsuji M, Purushothama C, Tanaka K, Sano T (2012) Oligo-DNA custom macroarray for monitoring major pathogenic and non-pathogenic fungi and bacteria in the phyllosphere of apple trees. Plos One 7:e34249

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hill T, Walsh K, Harris J, Moffett B (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hillebrand H, Bennett D, Cadotte M (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520

    Article  PubMed  Google Scholar 

  • Hoshino Y, Matsumoto N (2007) Changes in fungal community structure in bulk soil and spinach rhizosphere soil after chemical fumigation as revealed by 18S rDNA PCR-DGGE. Soil Sci Plant Nutr 53:40–55

    Article  CAS  Google Scholar 

  • Hoshino YT, Morimoto S (2008) Comparison of 18S rDNA primers for estimating fungal diversity in agricultural soils using polymerase chain reaction-denaturing gradient gel electrophoresis. Soil Sci Plant Nutr 54:701–710

    Article  CAS  Google Scholar 

  • IFOAM (1972) Principles of organic agriculture. Available: http://www.ifoam.org/en/organic-landmarks/principles-organic-agriculture

  • Jangid K, Williams M, Franzluebbers A, Sanderlin J, Reeves J, Jenkins M, Endale D, Coleman D, Whitman W (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40:2843–2853

    Article  CAS  Google Scholar 

  • Jangid K, Williams M, Franzluebbers A, Schmidt T, Coleman D, Whitman W (2011) Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem 43:2184–2193

    Article  CAS  Google Scholar 

  • Johnsen K, Jacobsen C, Torsvik V, Sorensen J (2001) Pesticide effects on bacterial diversity in agricultural soils—a review. Biol Fertil Soils 33:443–453

    Article  CAS  Google Scholar 

  • Jonsson L, Nilsson M, Wardle D, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364

    Article  Google Scholar 

  • Konopka A (2009) What is microbial community ecology? ISME J 3:1223–1230

    Article  PubMed  Google Scholar 

  • Korthals G, Alexiev A, Lexmond T, Kammenga J, Bongers T (1996) Long-term effects of copper and pH on the nematode community in an agroecosystem. Environ Toxicol Chem 15:979–985

    Article  CAS  Google Scholar 

  • Kuramae E, Yergeau E, Wong L, Pijl A, van Veen J, Kowalchuk G (2012) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79:12–24

    Article  CAS  PubMed  Google Scholar 

  • Kuramae E, Hillekens R, de Hollander M, van der Heijden M, van den Berg M, van Straalen N, Kowalchuk G (2013) Structural and functional variation in soil fungal communities associated with litter bags containing maize leaf. FEMS Microbiol Ecol 84:519–531

    Article  CAS  PubMed  Google Scholar 

  • Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace I, Wilm A, Lopez R, Thompson J, Gibson T, Higgins D (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Mader P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697

    Article  CAS  PubMed  Google Scholar 

  • MAFF (2010) Recommended rate of fertilizer application, Tokyo, Japan. Available: http://www.maff.go.jp/j/seisan/kankyo/hozen_type/h_sehi_kizyun. (in Japanese)

  • May LA, Smiley B, Schmidt MG (2001) Comparative denaturing gradient gel electrophoresis analysis of fungal communities associated with whole plant corn silage. Can J Microbiol 47:829–841

    Article  CAS  PubMed  Google Scholar 

  • Moeskops B, Sukristiyonubowo BD, Sleutel S, Herawaty L, Husen E, Saraswati R, Setyorini D, De Neve S (2010) Soil microbial communities and activities under intensive organic and conventional vegetable farming in West Java, Indonesia. Appl Soil Ecol 45:112–120

    Article  Google Scholar 

  • Morimoto S, Hayatsu M, Takada Hoshino Y, Nagaoka K, Yamazaki M, Karasawa T, Takenaka M, Akiyama H (2011) Quantitative analyses of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in fields with different soil types. Microbes Environ 26:248–253

    Article  PubMed  Google Scholar 

  • Mulder C, De Zwart D, Van Wijnen H, Schouten A, Breure A (2003) Observational and simulated evidence of ecological shifts within the soil nematode community of agroecosystems under conventional and organic farming. Funct Ecol 17:516–525

    Article  Google Scholar 

  • Naeem S (2009) Ecology: Gini in the bottle. Nature 458:579–580

    Article  CAS  PubMed  Google Scholar 

  • Nakai M (2006) The present conditions and problem of investigation on arable soils. Agric 31–42 (in Japanese)

  • Neera P, Katano M, Hasegawa T (1999) Comparison of rice yield after various years of cultivation by natural farming. Plant Prod Sci 2:58–64

    Article  Google Scholar 

  • Nishizawa T, Zhaorigetu KM, Sato Y, Kaneko N, Ohta H (2010) Molecular characterization of fungal communities in non-tilled, cover-cropped upland rice field soils. Microbes Environ 25:204–210

    Article  PubMed  Google Scholar 

  • Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675

    Article  CAS  Google Scholar 

  • Okada H, Harada H (2007) Effects of tillage and fertilizer on nematode communities in a Japanese soybean field. Appl Soil Ecol 35:582–598

    Article  Google Scholar 

  • Okada H, Oba H (2008) Comparison of nematode community similarities assessed by polymerase chain reaction-denaturing gradient gel electrophoresis (DGGE) and by morphological identification. Nematol 10:689–700

    Article  CAS  Google Scholar 

  • Omar S, Abdel-Sater M (2001) Microbial populations and enzyme activities in soil treated with pesticides. Water Air Soil Pollut 127:49–63

    Article  CAS  Google Scholar 

  • Orr C, Leifert C, Cummings S, Cooper J (2012) Impacts of organic and conventional crop management on diversity and activity of free-living nitrogen fixing bacteria and total bacteria are subsidiary to temporal effects. Plos One 7:e52891

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.r-project.org

  • Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reganold J, Glover J, Andrews P, Hinman H (2001) Sustainability of three apple production systems. Nature 410:926–930

    Article  CAS  PubMed  Google Scholar 

  • Sano S, Yanai J, Kosaki T (2004) Evaluation of soil nitrogen status in Japanese agricultural lands with reference to land use and soil types. Soil Sci Plant Nutr 50:501–510

    Article  CAS  Google Scholar 

  • Sano S, Uchiyama T, Tatsui M (2010) Evaluation of agricultural soil properties and organic material management in urban areas, Osaka Prefecture in Japan. World Congress of Soil Science, Soil Solutions for a Changing World1 – 6 August 2010, Brisbane, Australia

  • Srinivasan M, Laxman R, Deshpande M (1991) Physiology and nutritional aspects of Actinomycetes: an over view. World J Microbiol Biotechnol 7:171–184

    Article  CAS  PubMed  Google Scholar 

  • Strickland M, Rousk J (2010) Considering fungal: bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  CAS  Google Scholar 

  • Sugiyama S (2013) Marvelous soil in a miracle apple filed: ecological perspectives on natural farming system. Gentosha, Tokyo (in Japanese)

    Google Scholar 

  • Sugiyama A, Vivanco J, Jayanty S, Manter D (2010) Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms. Plant Dis 94:1329–1335

    Article  CAS  Google Scholar 

  • Sun H, Deng S, Raun W (2004) Bacterial community structure and diversity in a century-old manure-treated agroecosystem. Appl Environ Microbiol 70:5868–5874

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suzuki C, Nagaoka K, Shimada A, Takenaka M (2009) Bacterial communities are more dependent on soil type than fertilizer type, but the reverse is true for fungal communities. Soil Sci Plant Nutr 55:80–90

    Article  CAS  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    Article  CAS  PubMed  Google Scholar 

  • Torsvik V, Ovreas L, Thingstad T (2002) Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296:1064–1066

    Article  CAS  PubMed  Google Scholar 

  • van Bruggen A, Semenov A (2000) In search of biological indicators for soil health and disease suppression. Appl Soil Ecol 15:13–24

    Article  Google Scholar 

  • van der Heijden M, Bardgett R, van Straalen N (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • van Diepeningen A, de Vos O, Korthals G, van Bruggen A (2006) Effects of organic versus conventional management on chemical and biological parameters in agricultural soils. Appl Soil Ecol 31:120–135

    Article  Google Scholar 

  • Waite IS, O’Donnell AG, Harrison A, Davies JT, Colvan SR, Ekschmitt K, Dogan H, Wolters V, Bongers T, Bongers M, Bakonyi G, Nagy P, Papatheodorou EM, Stamou GP, Bostrom S (2003) Design and evaluation of nematode 18S rDNA primers for PCR and denaturing gradient gel electrophoresis (DGGE) of soil community DNA. Soil Biol Biochem 35:1165–1173

    Article  CAS  Google Scholar 

  • Wardle D, Bardgett R, Klironomos J, Setala H, van der Putten W, Wall D (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Wu T, Chellemi D, Martin K, Graham J, Rosskop E (2007) Discriminating the effects of agricultural land management practices on soil fungal communities. Soil Biol Biochem 39:1139–1155

    Article  CAS  Google Scholar 

  • Yamamura K (1999) Transformation using (x + 0.5) to stabilize the variance of populations. Res Popul Ecol 41:229–234

    Article  Google Scholar 

  • Yeates G (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fertil Soils 37:199–210

    Google Scholar 

  • Yeates G, Bardgett R, Cook R, Hobbs P, Bowling P, Potter J (1997) Faunal and microbial diversity in three Welsh grassland soils under conventional and organic management regimes. J Appl Ecol 34:453–470

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the owners of the Orchard-N and the Orchard-C. The authors are also grateful to Sho Morimoto, Yoriko Sakai, and Yumi Shimomura in qPCR analysis and Sunao Kikuchi in the analysis of total C, total N, and available PO4-P. This study was supported by a Grant-in-Aid (Soil eDNA project) from the Ministry of Agriculture, Forestry and Fisheries of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seiya Tsushima.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 130 kb)

ESM 2

(PDF 121 kb)

ESM 3

(PDF 121 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsushita, Y., Bao, Z., Kurose, D. et al. Community structure, diversity, and species dominance of bacteria, fungi, and nematodes from naturally and conventionally farmed soil: a case study on Japanese apple orchards. Org. Agr. 5, 11–28 (2015). https://doi.org/10.1007/s13165-015-0096-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13165-015-0096-4

Keywords

Navigation