While root exudation follows diurnal rhythms, little is known about the consequences for the microbiome of the rhizosphere. In this study, we used a metatranscriptomic approach to analyze the active microbial communities, before and after sunrise, in the rhizosphere of barley. We detected increased activities of many prokaryotic microbial taxa and functions at the pre-dawn stage, compared to post-dawn. Actinomycetales, Planctomycetales, Rhizobiales, and Burkholderiales were the most abundant and therefore the most active orders in the barley rhizosphere. The latter two, as well as Xanthomonadales, Sphingomonadales, and Caulobacterales showed a significantly higher abundance in pre-dawn samples compared to post-dawn samples. These changes in taxonomy coincide with functional changes as genes involved in both carbohydrate and amino acid metabolism were more abundant in pre-dawn samples compared to post-dawn samples. This study significantly enhances our present knowledge on how rhizospheric microbiota perceives and responds to changes in the soil during dark and light periods.
We thank Luhua Yang for the advice on germination and planting of the barley seeds and J. BarbroWinkler for technical advice in the greenhouse. We thank European Marie Curie ITN for funding Divyashri Baraniya and Anne Schöler through “TRAINBIODIVERSE” project, grant No. 289949. Gisle Vestergaard is supported by a Humboldt Research Fellowship for postdoctoral researchers.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
ESM 2Supplementary Fig. 2 (S2): The most abundant bacterial orders of significantly different KEGG pathways. Depicted are the ten most abundant bacterial orders in percentages of reads for the pathways, which were more active at pre-dawn (carbohydrate metabolism, nucleotide metabolism, amino acid metabolism and metabolism of cofactors and vitamins). Significant differences between pre-dawn and post-dawn time points were determined by unpaired t-test statistics (∗P < 0.05, n = 3). (PDF 362 kb)
ESM 3Supplementary Table 1 Pre-processing of Illumina mRNA reads. Supplementary Table 2 Relative abundance of reads belonging to taxonomic classes which were significantly different between day and night. Supplementary Table 3 Relative abundance of reads belonging to KEGG pathways which were significantly different between day and night (DOCX 24 kb)
Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148PubMedPubMedCentralGoogle Scholar
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefPubMedGoogle Scholar
Brzostek ER, Greco A, Drake JE, Finzi AC (2013) Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115:65–76CrossRefGoogle Scholar
Kuzyakov Y, Cheng W (2004) Photosynthesis controls of CO2 efflux from maize rhizosphere. Plant Soil 263:85–99CrossRefGoogle Scholar
Töwe S, Wallisch S, Bannert A, Fischer D, Hai B, Haesler F, et al. (2011) Improved protocol for the simultaneous extraction and column-based separation of DNA and RNA from different soils. J Microbiol Methods 84:406–412CrossRefPubMedGoogle Scholar
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, et al. (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403CrossRefPubMedPubMedCentralGoogle Scholar
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 11:1358–1375CrossRefPubMedGoogle Scholar
Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A, et al. (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant-Microbe Interact 14:775–784CrossRefPubMedGoogle Scholar
Iijima M, Sako Y, Rao TP (2003) A new approach for the quantification of root-cap mucilage exudation in the soil. Plant Soil 225:399–407CrossRefGoogle Scholar
Lünsmann V, Kappelmeyer U, Taubert A, Nijenhuis I, Von Bergen M, Heipieper HJ, et al. (2016) Aerobic toluene degraders in the rhizosphere of a constructed wetland model show diurnal polyhydroxyalkanoate metabolism. Appl Environ Microbiol 82:4126–4132CrossRefPubMedPubMedCentralGoogle Scholar
Ishikawa CM, Bledsoe CS (2000) Seasonal and diurnal patterns of soil water potential in the rhizosphere of blue oaks: evidence for hydraulic lift. Oecologia 125:459–465CrossRefPubMedGoogle Scholar
Matimati I, Anthony Verboom G, Cramer MD (2014) Do hydraulic redistribution and nocturnal transpiration facilitate nutrient acquisition in Aspalathus linearis? Oecologia 175:1129–1142CrossRefPubMedGoogle Scholar
Cardon ZG, Gage DJ (2006) Resource exchange in the rhizosphere: molecular tools and the microbial perspective. Annu Rev Ecol Evol Syst 37:459–488CrossRefGoogle Scholar