Abstract
Aims
Study of the microbial expression profile in the rhizosphere of two contrasting maize lines, differing in the Nitrogen Use efficiency (NUE).
Methods
The Lo5 and T250 inbred maize characterized by high and low NUE, respectively, were grown in rhizoboxes allowing precise sampling of rhizosphere and bulk soils. We conducted metatranscriptomic of rhizosphere and bulk soil by m-RNA sequencing.
Results
High activity of bacteria was observed compared to archaea and fungi in both rhizosphere and bulk soils of both maize lines. Proteobacteria and Actinobacteria were involved in all processes, while significant shifts occurred in the expression of Bacteroidetes, Chloroflexi, Firmicutes, Acidobacteria, Cyanobacteria, archaea and fungi, indicating their possible role in specific processes occurring in rhizosphere of two maize lines. Maize plants with different NUE induced changes in microbial processes, especially in N cycling, with high NUE maize favouring ammonification and nitrification processes and low NUE maize inducing expression of genes encoding for denitrifying process, likely favoured by longer N residence time in the rhizosphere.
Conclusions
Overall our results showed that maize lines with different NUE shaped not only microbial communities but also conditioned the microbial functions and the N cycle in their rhizosphere. While the plant NUE is genetically determined and an inherent plant physiological trait, it also stimulates changes in the microbial community composition and gene expression in the rhizosphere, favouring microbial processes that mineralize and oxidize N in the high NUE maize. These results can improve our understanding on plant-microbe interaction in the rhizosphere of crop plants with potential applications for improving the management practices of the agro-ecosystems.
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References
Aira M, Gómez-Brandón M, Lazcano C, Bääth E, Domínguez J (2010) Plant genotype strongly modified the structure and growth of maize rhizosphere microbial communities. Soil Biol Biochem 42:2276–2281
Aislabie J, Deslippe JR (2013) Soil microbes and their contribution to soil services. In dymond JRed. Ecosystem services in New Zealand – Condition and trend. Manaaki Whenual press, Lincon. NewZealand pp-143:161
Baraniya D, Puglisi E, Ceccherini MT, Pietramellara G, Giagnoni L, Arenella MR, Nannipieri P, Renella G (2016) Protease encoding microbial communities and protease activity of therhizosphere and bulk soils of two maize lines with different N uptake efficiency. Soil Biol Biochem 96:176–179
Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soiland maize rhizosphere. Soil Biol Biochem 35:1183–1192
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Bland C, Armengaud J (2014) Proteogenomics: a new integrative approach for a better description of protein diversity found in soil microflora. In Nannipieri P, Pietramellara G, Renella G (eds) Omics in soil science. Caister Academic Press, UK, pp 139–162
Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:43–50
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bray JR, Curtis JT (1957) An ordination of upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349
Brimecombe MJ, De Leij FAAM, Lynch JM (2007) Rhizodeposition and microbial populations. In: Pinton, R., Varanini, Z., Nannipieri, P. (Eds.), The Rhizosphere: Biochemistry and Organic Sub-stances at the Soil-plant Interface. CRC Press, Taylor & Francis Group, Boca Raton, London, New York, pp. 73–109
Carvalhais LC, Dennis PG, Tyson GW, Schenk PM (2012) Application of metatranscriptomics to soil environments. J Microbiol Meth 91:246–251
Chauhan A, Smartt A, Wang J, Utturkar S, Frank A, Bi M et al (2014) Integrated metagenomics and metatranscriptomics analyses of root-associated soil from transgenic switchgrass. Genome Announc 2(4):e00777–e00714
Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263
Damon C, Lehembre F, Oger-Desfeux C, Luis P, Ranger J, Fraissinet-Tachet L, Marmeisse R (2012) Metatranscriptomics reveals the diversity of genes expressed by eukaryotes in forest soils. PLoS One 7:e28967
Dohrmann AB, Kuting M, Junemann S, Jaenicke S, Schluter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt- and conventional maize varieties. ISME J 7:37–49
Etchebehere C, Errazquin MI, Dabert P, Moletta R, Muxi L (2001) Comamonas nitrativorans sp. nov., a novel denitrifier isolated from a denitrifying reactor treating landfill leachate. Int J Syst Evol Microbiol 51:977–983
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364
Giagnoni L, Magherini F, Landi L, Taghavi S, Modesti A, Bini L, Nannipieri P, van der lelie D, Renella G (2011) Extraction of microbial proteome from soil: potential and limitations assessed through a model study. Eur J Soil Sci 62:74–81
Giagnoni L, Magherini F, Landi L, Taghavi S, van der Lelie D, Puglia M, Bianchi L, Bini L, Nannipieri P, Renella G, Modesti A (2012) Soil solid phases effects on the proteomic analysis of Cupriavidus metallidurans CH34. Biol Fertil Soils 48:425–433
Giagnoni L, Pastorelli R, Mocali S, Arenella M, Nannipieri P, Renella G (2016) Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency. Appl Soil Ecol 98:30–38
Gumaelius L, Magnusson G, Petterson B, Dalhammar G (2001) Comamonas denitrificans sp. nov. an efficient denitrifying bacterium isolated from activated sludge. Int J Syst Evol Microbiol 51:999–1006
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistic software package for education and data analysis. Palaeontol Electron 4:1–9
He Y, Hu W, Ma D, Lan H, Yang Y, Gao Y (2017) Abundance and diversity of ammonia-oxidising archaea and bacteria in the rhizosphere soil of three plants in Ebinur lake wetland. Can J Microbiol 63:573:582
Howe AC, Jansson JK, Malfatti SA, Tringe SG, Tiedje JM, Brown CT (2014) Tackling soil diversity with the assembly of large, complex metagenomes. Proc Natl Acad Sci 111:4904–4909
Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728
Jonczyk R, Schmidt H, Osterrieder A, Fiesselmann A, Schullehner K, Haslbeck M, Sicker D, Hofmann D, Yalpani N, Simmons C, Frey M, Gierl A (2008) Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiol 146:1053–1063
Kielak A, Pijl AG, van Veen JA, Kowalchuk G (2009) Phylogenetic diversity of Acidobacteria in former agricultural soil. ISME J 3:378–382
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:10
Li X, Rui J, Xiong J, Li J, He Z, Zhou J, Yannarell AC, Mackie RI (2014a) Functional potential of soil microbial communities in the maize rhizosphere. PLoS One 9(11):e112609
Li X, Rui J, Mao Y, Yannarell A, Mackie R (2014b) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401
Lynch JM (1990) Introduction: some consequences of microbial rhizosphere competence for plant and soil. In: Lynch JM (ed) The rhizosphere. John Wiley, Chichester, pp 1–10
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386
Moran AM (2009) Metatranscriptomics: eavesdropping on complex microbial communities. Microbe 4:329–335
Nacke H, Fischer C, Thurmer A, Meinicke P, Daniel R (2014) Land use type significantly affects microbial gene transcription in soil. Microb Ecol 67:919–930
Nannipieri P (2014) Soil as biological system. In: Nannipieri P, Pietramellara G, Renella G (Eds)., omics in soil science. Caister Academic Press, U.K, pp 1–7
Pathan SI, CeccheriniMT PG, Puschenreiter M, Giagnoni L, Arenella M et al (2015a) Enzyme activity and microbial community structure in the rhizosphere of two maize lines differing in N use efficiency. Plant Soil 387:413–424
Pathan SI, Ceccherini MT, Hansen MA, Giagnoni L, Ascher J, Arenella M, Sørensen SJ, Pietramellara G, Nannipieri P, Renella G (2015b) Maize lines with different nitrogen use efficiency (NUE) also differ for molecular diversity of bacterial β-glucosidase gene and glucosidase activity in their rhizosphere. Biol Fertil Soils 51:995–1004
Patureau D, Bernet N, Moletta R (1996) Study of the denitrifying enzymatic system of comamonas sp. strain SGLY2 under various aeration condition with particular view on nitrate and nitrite reductase. Curr Microbiol 32:25–32
Peiffera JA, Sporb A, Korenb O, Jinb Z, Tringed SG, Dangle JL et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 110:6548–6553
Pell J, Hintze A, Canino-Koning R, Howe A, Tiedje JM, Brown CT (2012) Scaling metagenome sequence assembly with probabilistic de Bruijn graphs. Proc Natl Acad Sci 109:13272–13277
Philippot S, Halin S, Börhesson G, Baggs EM (2009) Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81
Poretsky RS, Hewson I, Sun S, Allen AE, Zehr JP, Moran MA (2009) Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre. Environ Microbiol 11:1358–1375
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject.org
Renella G, Landi L, Valori F, Nannipieri P (2007) Microbial and hydrolase activity after release of low molecular weight organic compounds by a model root surface in a clayey and a sandy soil. Appl Soil Ecol 36:124–129
Robertson CE, Harris JK, Spear JR, Pace NR (2005) Phylogenetic diversity and ecology of environmental archaea. Curr Opin Microbiol 8:638–642
Saia S, Ruisi P, Fileccia V, Di Miceli G, Amato G, Martinelli F (2015) Metabolomics suggests that soil inoculation with arbuscular mycorrhizal fungi decreased free amino acid content in roots of durum wheat grown under N-limited. P-rich field conditions. PLoS One 10:e0129591
Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489
Urich T, Lanzèn A, Qi J, Huson DH, Schleper C, Schuster SC (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS One 3(6):e2527
Varanini Z, Cesco S, Tomasi N, Pinton R, Guzzo F, Zamboni A, Schloter-Hai B, Schloter M, Giagnoni L, Arenella M, Nannipieri P, Renella G (2018) Nitrate induction and physiological responses of two maize lines differing in nitrogen use efficiency: effects on N availability, microbial diversity and enzyme activity in the rhizosphere. Plant Soil 422:331–347
Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart: how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–584
Villagrasa M, Guillamón M, Navarro A, Eljarrat E, Barceló D (2008) Development of a pressurized liquid extractions solid-phase extraction followed by liquid chromatography-electrospray ionization tandem mass spectrometry method for the quantitative determination of benzoxazolinones and their degradation products in agricultural soil. J Chromatogr A 1179:190–197
WRB World Reference Base for Soil Resources (1998) World soil resources reports 84. FAO, Rome
Zamboni A, Astolfi S, Zuchi S, Pii Y, Guardini K, Tononi P, Varanini Z (2014) Nitrate induction triggers different transcriptional changes in a high and a low nitrogen use efficiency maize inbred line. J Integr Plant Biol 56:1080–1094
Zhang WW, Andong ZY, Zhang M, Wang QN, Wei YQ, Chen LX (2014) Isolation and characterization of a heterotrophic nitrifier Proteus mirabilis strain V7 and its potential application in NH4 +-N removal. Ann Microbiol 64:1231–1238
Žifčáková L, Větrovsky T, Adina CH, Baldrian P (2016) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Env Microbiol 18:288–301
Žifčáková L, Větrovský T, Lombard V, Henrissat B, Howe A, Baldrian P (2017) Feed in summer, rest in winter: microbial carbon utilization in forest topsoil. Microbiome 5(1):122
Acknowledgments
This research was supported by the Ministry for Education and Research project “PRIN 2009MWY5F9”. Shamina Imran Pathan was supported by the Marie Curie ITN action “TRAINBIODIVERSE”, grant no. 289949. The Department of Agrifood Production and Environmental Sciences thanks to the Ente Cassa di Risparmio di Firenze for the financial support for the acquisition of new instruments. Moreover, we would like to thank Editor and anonymous Reviewer for their valuable suggestions.
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Pathan, S.I., Větrovský, T., Giagnoni, L. et al. Microbial expression profiles in the rhizosphere of two maize lines differing in N use efficiency. Plant Soil 433, 401–413 (2018). https://doi.org/10.1007/s11104-018-3852-x
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DOI: https://doi.org/10.1007/s11104-018-3852-x