Archives of Microbiology

, Volume 199, Issue 2, pp 303–315 | Cite as

Comparative study of rhizobacterial communities in pepper greenhouses and examination of the effects of salt accumulation under different cropping systems

  • Mi-Seon Hahm
  • Jin-Soo Son
  • Byung-Soo Kim
  • Sa-Youl Ghim
Original Paper

Abstract

This study compared rhizobacterial communities in pepper greenhouses under a paddy-upland (rice–pepper) rotational system (PURS) and a monoculture repeated cropping system (RCS) and examined adverse effects of high salinity on soil properties. The following soil properties were analyzed: electrical conductivity (EC), pH, concentration of four cations (Na, Ca, Mg, and K), total nitrogen, and organic matter content. Rhizobacterial communities were analyzed using culture-based and culture-independent (pyrosequencing) methods. In addition, all culturable bacteria isolated from each soil sample were tested for traits related to plant growth promotion. The EC of rhizospheric soils was 5.32–5.54 dS/m for the RCS and 2.05–2.19 dS/m for the PURS. The culture-based method indicated that the bacterial communities and bacterial characteristics were significantly more diverse in the PURS soil than in the RCS soil. The pyrosequencing data also indicated that the richness and diversity of bacterial communities were greater in the PURS soil. Proteobacteria was the most abundant phylum in soil samples under both cropping systems. However, Firmicutes and Gemmatimonadetes were more prevalent in the RCS soil, while the PURS soil contained a greater number of Chloroflexi. Spearman’s correlation coefficients showed that soil EC was significantly positively correlated with the abundance of Firmicutes and Gemmatimonadetes and negatively correlated with the abundance of Acidobacteria, Chloroflexi, and Deltaproteobacteria. This is the first study on the rhizobacterial communities in pepper greenhouses under two different cropping systems using both culture- and pyrosequencing-based methods.

Keywords

16S rRNA Cropping system Pyrosequencing Rhizobacterial communities Soil bacterial diversity 

Abbreviations

RCS

Repeated cropping system

PURS

Paddy-upland rotational system

References

  1. Aanderud ZT, Lennon JT (2011) Validation of heavy-water stable isotope probing for the characterization of rapidly responding soil bacteria. Appl Environ Microbiol 77:4589–4596CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ambrosini A, Beneduzi A, Stefanski T, Pinheiro FG, Vargas LK, Passaglia LMP (2012) Screening of plant growth promoting rhizobacteria isolated from sunflower (Helianthus annuus L.). Plant Soil 356:245–264CrossRefGoogle Scholar
  3. Arruda L, Beneduzi A, Martins A, Lisboa B, Lopes C, Bertolo F, Passaglia LMP, Vargas LK (2013) Screening of rhizobacteria isolated from maize (Zea mays L.) in Rio Grande do Sul State (South Brazil) and analysis of their potential to improve plant growth. Appl Soil Ecol 63:15–22CrossRefGoogle Scholar
  4. Beneduzi A, Moreira F, da Costa PB, Vargas LK, Lisboa BB, Favreto R, Baldani JI, Passaglia LMP (2013) Diversity and plant growth promoting evaluation abilities of bacteria isolated from sugarcane cultivated in the South of Brazil. Appl Soil Ecol 63:94–104CrossRefGoogle Scholar
  5. Carbonetto B, Rascovan N, Álvarez R, Mentaberry A, Vázquez MP (2014) Structure, composition and metagenomic profile of soil microbiomes associated to agricultural land use and tillage systems in argentine pampas. PLoS One 9:e99949CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261CrossRefPubMedGoogle Scholar
  7. Costello EK, Schmidt SK (2006) Microbial diversity in alpine tundra wet meadow soil: novel Chloroflexi from a cold, water-saturated environment. Environ Microbiol 8:1471–1486CrossRefPubMedGoogle Scholar
  8. De Souza R, Beneduzi A, Ambrosini A, da Costa PB, Meyer J, Vargas KL, Schoenfeld R, Passaglia LMP (2013) The effect of plant growth-promoting rhizobacteria on the growth of rice (Oryza sativa L.) cropped in southern Brazilian fields. Plant Soil 366:585–603CrossRefGoogle Scholar
  9. DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77:6295–6300CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crc Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  11. Drees KP, Neilson JW, Betancourt JL, Quade J, Henderson DA, Pryor BM, Maier RM (2006) Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl Environ Microbiol 72:7902–7908CrossRefPubMedPubMedCentralGoogle Scholar
  12. Edgar RC, Haas BJ, Clemente JC, Quincec C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  13. Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7CrossRefPubMedCentralGoogle Scholar
  14. Farina R, Beneduzi A, Ambrosini A, de Campos SB, Lisboa BB, Wendisch V, Vargas LK, Passaglia LMP (2012) Diversity of plant growth-promoting rhizobacteria communities associated with the stages of canola growth. Appl Soil Ecol 55:44–52CrossRefGoogle Scholar
  15. Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796PubMedPubMedCentralGoogle Scholar
  16. Hahm MS, Sumayo M, Hwang YJ, Jeon SA, Park SJ, Lee JY, Ahn JH, Kim BS, Ryu CM, Ghim SY (2012) Biological control and plant growth promoting capacity of rhizobacteria on pepper under greenhouse and field conditions. J Microbiol 50:380–385CrossRefPubMedGoogle Scholar
  17. Hameeda B, Harini G, Rupela OP, Wani SP, Reddy G (2008) Growth promotion of maize by phosphate-solubilizing bacteria isolated from composts and macrofauna. Microbiol Res 163:234–242CrossRefPubMedGoogle Scholar
  18. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  19. Hong EH, Lee SH, Vendan RT, Rhee YH (2012) Molecular diversity of rhizobacteria in ginseng soil and their plant benefiting attributes. Korean J Microbiol 48:246–253CrossRefGoogle Scholar
  20. Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480CrossRefPubMedGoogle Scholar
  21. Kim M, Yoon H, Kim YE, Kim YJ, Kong WS, Kim JG (2014) Comparative analysis of bacterial diversity and communities inhabiting the fairy ring of Tricholoma matsutake by barcoded pyrosequencing. J Appl Microbiol 117:699–710CrossRefPubMedGoogle Scholar
  22. Kloepper JW, Schoroth MN (1978) Plant growth-promoting rhizobacteria on radishes. Proc IVth Int Conf 2:879–882Google Scholar
  23. 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 Microbiol 75:5111–5120CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lea-Cox JD, Syvertsen JP (1992) Salinity increases nitrogen leaching losses from citrus in sandy soil. Proc Fla State Hort Soc 105:76–82Google Scholar
  25. Lee KS (1997) Evaluation on the effects of pesticide residues to agroecosystem in Korea. Korean J Environ Agric 16:80–93Google Scholar
  26. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659CrossRefPubMedGoogle Scholar
  27. Lugtenberg B, Kamilova F (2009) Plant growth promoting rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefPubMedGoogle Scholar
  28. Nakade DB (2013) Bacterial diversity in Sugarcane (Saccharum officinarum) rhizosphere of saline soil. Int Res J Biol Sci 2:60–64Google Scholar
  29. Narihiro T, Kamagata Y (2013) Cultivating yet-to-be cultivated microbes: the challenge continues. Microbes Environ 28:163–165CrossRefPubMedPubMedCentralGoogle Scholar
  30. Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate-solubilizing microorganisms. FEMS Microbiol Lett 170:265–270CrossRefPubMedGoogle Scholar
  31. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol R 64:548–572CrossRefGoogle Scholar
  32. Nocker A, Sossa-Fernandez P, Burr MD, Camper KA (2007) Use of propidium monoazide for live/dead distinction in microbial ecology. Appl Environ Microbiol 73:5111–5117CrossRefPubMedPubMedCentralGoogle Scholar
  33. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15CrossRefPubMedGoogle Scholar
  34. Pointing SB, Chan YK, Lacap DC, Lau MCY, Jurgens JA (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci 106:19964–19969CrossRefPubMedPubMedCentralGoogle Scholar
  35. Schwyn B, Neilands JB (1987) University chemical assay for the detection and determination of siderophore. Anal Biochem 160:46–52CrossRefGoogle Scholar
  36. Shannon CE (1948) The mathematical theory of communication. Bell Syst Tech J 27:379–423CrossRefGoogle Scholar
  37. Son JS, Sumayo M, Hwang YJ, Kim BS, Ghim SY (2014) Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl Soil Ecol 73:1–8CrossRefGoogle Scholar
  38. Sugiyama A, Ueda Y, Zushi T, Takase H, Yazaki K (2014) Changes in the bacterial community of soybean rhizospheres during growth in the field. PLoS One 9:e100709CrossRefPubMedPubMedCentralGoogle Scholar
  39. Unlukara A, Demir I, Kesmez D, Çelikkol T, Demir K (2013) Seed yield and quality of pepper plants grown under salt stress. Afr J Biotechnol 12:6833–6836Google Scholar
  40. Upadhyay SK, Singh DP, Saikia R (2009) Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Curr Microbiol 59:489–496CrossRefPubMedGoogle Scholar
  41. Uroz S, Ioannidis P, Lengelle J, Cébron A, Morin E, Buée M, Martin F (2013) Functional assays and metagenomic analyses reveals differences between the microbial communities inhabiting the soil horizons of a Norway spruce plantation. PLoS One 8:e55929CrossRefPubMedPubMedCentralGoogle Scholar
  42. Van Hoorn JW, Katerji N, Hamdy A, Mastrorilli M (2001) Effect of salinity on yield and nitrogen uptake of four grain legumes and on biological nitrogen contribution. Agric Water Manage 51:87–98CrossRefGoogle Scholar
  43. Wakelin SA, Anand RR, Reith F, Gregg AL, Noble RRP, Goldfarb KC, Andersen GL, DeSantis TZ, Piceno YM, Brodie EL (2012) Bacterial communities associated with a mineral weathering profile at a sulphidic mine tailings dump in arid Western Australia. FEMS Microbiol Ecol 79:298–311CrossRefPubMedGoogle Scholar
  44. Wong VNL, Greene RSB, Murphy BW, Dalal R, Mann S (2005) Decomposition of added organic material in salt-affected soils. In: Roach I (ed) Cooperative Research Centre for landscape environments and mineral exploration regional regolith symposia, 2nd–4th Nov. CRC LEME, CanberraGoogle Scholar
  45. Yu Z, Kraus TEC, Dahlgren RA, Horwath WR, Zasoski RJ (2003) Mineral and dissolved organic nitrogen dynamics along a soil acidity–fertility gradient. Soil Sci Soc Am J 67:878–888CrossRefGoogle Scholar
  46. Zhao J, Zhang R, Xue C, Xun W, Sun L, Xu Y, Shen Q (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microb Ecol 67:443–453CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Mi-Seon Hahm
    • 1
  • Jin-Soo Son
    • 1
  • Byung-Soo Kim
    • 2
  • Sa-Youl Ghim
    • 1
  1. 1.School of Life Science, BK21 Plus KNU Creative BioResearch Group, Institute for MicroorganismsKyungpook National UniversityDaeguKorea
  2. 2.Department of HorticultureKyungpook National UniversityDaeguKorea

Personalised recommendations