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Shifts of microbial communities of wheat (Triticum aestivum L.) cultivation in a closed artificial ecosystem

  • Applied microbial and cell physiology
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Abstract

The microbial communities of plant ecosystems are in relation to plant growing environment, but the alteration in biodiversity of rhizosphere and phyllosphere microbial communities in closed and controlled environments is unknown. The purpose of this study is to analyze the change regularity of microbial communities with wheat plants dependent-cultivated in a closed artificial ecosystem. The microbial community structures in closed-environment treatment plants were investigated by a culture-dependent approach, polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE), and Illumina Miseq high-throughput sequencing. The results indicated that the number of microbes decreased along with time, and the magnitude of bacteria, fungi, and actinomycetes were 107–108, 105, and 103–104 CFU/g (dry weight), respectively. The analysis of PCR-DGGE and Illumina Miseq revealed that the wheat leaf surface and near-root substrate had different microbial communities at different periods of wheat ecosystem development and showed that the relative highest diversity of microbial communities appeared at late and middle periods of the plant ecosystem, respectively. The results also indicated that the wheat leaf and substrate had different microbial community compositions, and the wheat substrate had higher richness of microbial community than the leaf. Flavobacterium, Pseudomonas, Paenibacillus, Enterobacter, Penicillium, Rhodotorula, Acremonium, and Alternaria were dominant in the wheat leaf samples, and Pedobacter, Flavobacterium, Halomonas, Marinobacter, Salinimicrobium, Lysobacter, Pseudomonas, Halobacillus, Xanthomonas, Acremonium, Monographella, and Penicillium were dominant populations in the wheat near-root substrate samples.

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References

  • Ali B, Sabri AN, Ljung K, Hasnain S (2009) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 48(5):542–547

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436

    Article  CAS  PubMed  Google Scholar 

  • Borodina EV, Tirranen LS (2003) High temperature effect on microflora of radish root-inhabited zone and nutrient solutions for radish growth. Adv Space Res 31(1):235–240

    Article  CAS  PubMed  Google Scholar 

  • Brighigna L, Montaini P, Favilli F, Carabez-Trejo A (1992) Role of the nitrogen-fixing bacterial microflora in the epiphytism of Tillandsia (Bromeliaceae). Am J Bot 79:723–727

    Article  Google Scholar 

  • Cui D, Wang J, Chen J, Zhao Y, Gao C (2005) The danger of Alternaria to the crops. Natural Science Journal of Harbin Normal University 21(3):87–91

    Google Scholar 

  • Despommier D (2009) The rise of vertical farms. Sci Am 301:80–87

    Article  PubMed  Google Scholar 

  • Despommier D (2013) Farming up the city: the rise of urban vertical farms. Trends Biotechnol 31(7):388–389

    Article  CAS  PubMed  Google Scholar 

  • Dong C, Fu Y, Liu G, Liu H (2014a) Growth, photosynthetic characteristics, antioxidant capacity and biomass yield and quality of wheat (Triticum aestivum l.) exposed to led light sources with different spectra combinations. J Agron Crop Sci 200:219–230

    Article  CAS  Google Scholar 

  • Dong C, Hu D, Fu Y, Wang M, Liu H (2014b) Analysis and optimization of the effect of light and nutrient solution on wheat growth and development using an inverse system model strategy. Comput Electron Agric 109:221–231

    Article  Google Scholar 

  • Elizabeth MC, Malcolm BP, Sharon CC, William WK (2001) Antigenic characterization of the fish pathogen Flavobacterium psychrophilum. Appl Environ Microbiol 67(2):750–759

    Article  Google Scholar 

  • Ellis RJ, Morgan P, Weightman AJ, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metalcontaminated soil. Appl Environ Microbiol 69(6):3223–3230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elo S, Suominen I, Kämpfer P, Juhanoja J, Salkinoja-Salonen M, Haahtela K (2001) Paenibacillus borealis sp. Nov., a nitrogen-fixing species isolated from spruce forest humus in Finland. Int J Syst Evol Microbiol 51:535–545

    Article  CAS  PubMed  Google Scholar 

  • Ferris MJ, Ward DM (1997) Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis. Appl Environ Microbiol 63(4):1375–1381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y, Liu H (2012) Cultivation of three cruciferous vegetables in a confine environment decreases microbial burden. Ecol Eng 44:174–178

    Article  Google Scholar 

  • Fu Y, Liu H, Shao L, Wang M, Berkovich YA, Erokhin AN, Liu H (2013) A high-performance ground-based prototype of horn-type sequential vegetable production facility for life support system in space. Adv Space Res 52(1):97–104

    Article  CAS  Google Scholar 

  • Gitelson JI, Lisovsky GM, MacElroy RD (2002) Manmade closed ecological systems. Taylor & Francis, New York

    Google Scholar 

  • Gitelson JI, Tirranen LS, Borodina EV, Rygalov VY (1997) Impaired growth of plants cultivated in a closed system; possible reasons. Adv Space Res 20(10):1927–1930

    Article  CAS  PubMed  Google Scholar 

  • Graham MH, Haynes RJ (2005) Catabolic diversity of soil microbial communities under sugarcane and other land uses estimated by biology and substrate-induced respiration methods. Appl Soil Eco 29(2):155–164

    Article  Google Scholar 

  • Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3(4):307–319

    Article  CAS  PubMed  Google Scholar 

  • Hirano SS, Upper CD (2000) Bacteria in the leaf ecosytem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64(3):624–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang J, Jeong H, Yoe H (2014) Study on the plant factory automatic control system according to each crop growth step. Advanced Science and Technology Letters 49:174–179

    Google Scholar 

  • Ingela D, Harriet B, Staffan K (2000) rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecics heterigencity. Appl Environ Microbiol 66(8):3376–3380

    Article  Google Scholar 

  • Ladha JK, Barraquio WL, Watanabe I (1983) Isolation and identification of nitrogen-fixing Enterobacter cloacae and Klebsiella planticola associated with rice plants. Can J Microbiol 29(10):1301–1308

    Article  Google Scholar 

  • Lakshmanan V, Selvaraj G, Bais HP (2014) Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 166(2):689–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lasseur C, Verstraete W, Gros JB, Dubertret G, Rogalla F (1996) MELISSA: a potential experiment for a precursor mission to the Moon. Adv Space Res 18(11):111–117

    Article  CAS  PubMed  Google Scholar 

  • Li R (2011) The study of biocontrol on postharvest diseases of apples by Rhodotorula mucilaginosa and the possible mechanisms involved. Jiangsu University, Zhenjiang

    Google Scholar 

  • Li S, Jochum CC, Yu F, Zaleta-Rivera K, Du L, Harris SD, Yuen GY (2008) An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. Phytopathology 98(6):695–701

    Article  CAS  PubMed  Google Scholar 

  • Liang X, Fu Y, Tong L, Liu H (2014) Microbial shifts of the silkworm larval gut in response to lettuce leaf feeding. Appl Microbiol Biotechnol 98(8):3769–3776

    Article  CAS  PubMed  Google Scholar 

  • Lillian B, Nyckle JF, Bob S (1989) Effect of surface-active Pseudomonas spp. on leaf wettability. Appl Environ Microbiol 55(6):1340–1345

    Google Scholar 

  • Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69(4):1875–1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Littlefield-Wyer JG, Brooks P, Katouli M (2008) Application of biochemical fingerprinting and fatty acid methyl ester profiling to assess the effect of the pesticide Atradex on aquatic microbial communities. Environ Pollut 153(2):393–400

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Wang H, Yang H, Yi J, Zhou Y, Zhang N, Pang Z (2012a) Bacterial diversity of complete autotrophic nitrite-nitrification and electrochemical bio-denitrification combined process using PCR-DGGE. Chinese Journal of Environmental Engineering 6(9):3349–3355

    CAS  Google Scholar 

  • Liu H, Fu Y, Hu D, Hu E, Li L, Xie B (2012b) Bioregenerative life support systems in space: a research update. Science 338 (6104): 274-c, A Sponsored Supplement To Science: New Developments in Science and Technology - 60th Anniversary Special Issue, Beihang University (BUAA): 86–87

  • Logrieco A, Bottalico A, Mulé G, Moretti A, Perrone G (2003) Epidemiology of toxigenic fungi and their associated mycotoxins for some Mediterranean crops. Eur J Plant Pathol 109(7):645–667

    Article  CAS  Google Scholar 

  • Lytvynenko T, Zaetz I, Voznyuk T, Kovalchuk M, Rogutskyy I, Mytrokhyn O, Lukashov D, Estrella-Liopis V, Borodinova T, Mashkovska S, Foing B, Kordyum V, Kozyrovska N (2006) A rationally assembled microbial community for growing Tagetes patula L. in a lunar greenhouse. Res Microbiol 157(1):87–92

    Article  PubMed  Google Scholar 

  • Malcolm RS, Garrick CML, Mark CJ (1985) Acremonium fungal endophytes of tall fescue and perennial ryegrass: significance and control. Kentucky Agricultural Experiment Station Journal Series Paper 69(2):179–183

    Google Scholar 

  • Muyzer G (1999) DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2(3):317–322

    Article  CAS  PubMed  Google Scholar 

  • Muyzer G, dEC W, AG U (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Myers RM, Fischer SG, Lerman LS, Maniatis T (1985) Nearly all single base substitutions in DNA fragments joined to a GC-clamp can be detected by denaturing gradient gel electrophoresis. Nucleic Acids Res 13(9):3131–3145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Postgate J (1994) The outer reaches of life. Cambridge University Press, Cambridge

    Google Scholar 

  • Roberts MS, Garland JL, Mills AL (2004) Microbial astronauts: assembling microbial communities for advanced life support systems. Microb Ecol 47(2):137–149

    Article  CAS  PubMed  Google Scholar 

  • Roeland LB, Corene MJP, Peter AHMB (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486

    Article  Google Scholar 

  • Shimizu H, Saito Y, Nakashima H, Miyasaka J, Ohdoi K (2011) Light environment optimization for lettuce growth in plant factory. Paper presented at the Preprints of the 18th IFAC World Congress

  • Somova LA, Pechurkin NS, TI P (2005) Principles of biological adaptation of organisms in artificial ecosystems to changes of environmental factors. Adv Space Res 35:1512–1515

    Article  CAS  PubMed  Google Scholar 

  • Stanwood JM, Dighton J (2011) Seasonality and management, not proximity to highway, affect species richness and community composition of epiphytic phylloplane fungi found on (wild and cultivated) Vaccinium spp. Fungal Ecol 4(4):277–283

    Article  Google Scholar 

  • Strayer RF (1994) Dynamics of microorganism populations in recirculating nutrient solutions. Adv Space Res 14(11):357–366

    Article  CAS  PubMed  Google Scholar 

  • Tapia AA (2014) High-throughput sequencing of microbial communities in Poro cheese, an artisanal Mexican cheese. Food Microbiol 44:136–141

    Article  Google Scholar 

  • Teske A, Wawer C, Muyzer G, Ramsing NB (1996) Distribution of sulfate-reducing bacteria in a stratified fjord (Mariager Fjord, Denmark) as evaluated by most-probable-number counts and denaturing gradient gel electrophoresis of PCR-amplified ribosomal DNA fragments. Appl Environ Microbiol 62(4):1405–1415

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tirranen LS (2001) Formation of higher plant component microbial community in closed ecological system. Acta Astronaut 49(1):47–52

    Article  CAS  PubMed  Google Scholar 

  • Tirranen LS (2008) Microbiota of radish plants, cultivated in closed and open ecological systems. Acta Astronaut 63:1055–1060

    Article  CAS  Google Scholar 

  • Torsvik V, Daae FL, Sandaa RA, Ovreås L (1998) Novel techniques for analysing microbial diversity in natural and perturbed environments. J Biotechnol 64(1):53–62

    Article  CAS  PubMed  Google Scholar 

  • von der WI, Alviano DS, Santos AL, Soares RM, Alviano CS, Seldin L (2003) Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi. J Appl Microbiol 95(5):1143–1151

    Article  Google Scholar 

  • Wang G, Wang L, Zhang Y, Wang J, Xu X, Zhang C (2012a) Identification of an endophytic fungus of Ginkgo biloba TMSF169 and its antifungal metabolites. Chinese Journal of Biological Control 28(2):226–234

    Google Scholar 

  • Wang J, Liu P, Wang Y, Wang H, Li J, Zhuang Y, Zhu W (2012b) Antimicrobial aromatic polyketides from gorgonian-associated fungus, Penicillium commune 518. Chin J Chem 30(6):1236–1242

    Article  CAS  Google Scholar 

  • Yang C-H, David EC (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66(1):345–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuen GY, Steadman JR, Lindgren DT, Schaff D, Jochum C (2001) Bean rust biological control using bacterial agents. Crop Prot 20(5):395–402

    Article  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (No. 31301706).

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Authors and Affiliations

  1. Laboratory of Environmental Biology and Life Support Technology, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100191, China

    Youcai Qin, Yuming Fu, Chen Dong, Nannan Jia & Hong Liu

  2. Institute of Environmental Biology and Life Support Technology, Beihang University, Beijing, 100191, China

    Youcai Qin, Yuming Fu, Chen Dong, Nannan Jia & Hong Liu

  3. International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing, 100191, China

    Yuming Fu & Hong Liu

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  1. Youcai Qin
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  5. Hong Liu
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Correspondence to Yuming Fu or Hong Liu.

Ethics declarations

The study was approved by the Science and Ethics Committee of the School of Biological Science and Medical Engineering in Beihang University, Beijing, China (approval ID: 20140203, approval date: Jan. 15, 2014). This study was carried out in strict accordance and compliance with the Statement on Ethical Conduct in Research Involving Humans guidelines of the Science and Ethics Committee of the School of Biological Science and Medical Engineering in Beihang University.

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The authors declare that they have no competing interests.

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Youcai Qin and Chen Dong contributed equally to this work.

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Qin, Y., Fu, Y., Dong, C. et al. Shifts of microbial communities of wheat (Triticum aestivum L.) cultivation in a closed artificial ecosystem. Appl Microbiol Biotechnol 100, 4085–4095 (2016). https://doi.org/10.1007/s00253-016-7317-y

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  • DOI: https://doi.org/10.1007/s00253-016-7317-y

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