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Structure and Activity of Bacterial Community Inhabiting Rice Roots and the Rhizosphere

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Structure and Activity of Bacterial Community Inhabiting Rice Roots and the Rhizosphere Blackwell Publishing LtdOxford, UKEMIEnvironmental Microbiology 1462-2912© 2006 The Authors; Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd? 20068813511360Original ArticleBac- teria inhabiting rice roots and the rhizosphereY. Lu, D. Rosencrantz, W. Liesack and R. Conrad 中国科技论文在线 http://www.paper.edu.cn Environmental Microbiology (2006) 8(8), 1351–1360 doi:10.1111/j.1462-2920.2006.01028.x Structure and activity of bacterial community inhabiting rice roots and the rhizosphere 1,2 2 2 Yahai Lu, Dirk Rosencrantz, Werner Liesack and Plants, the primary producers, assimilate CO2 and distrib- Ralf Conrad2* ute the organic assimilates to the below-ground biota. The 1College of Resources and Environmental Sciences, below-ground biota, the degraders, transform the organic China Agricultural University, Beijing 100094, China. nutrients into inorganic compounds facilitating the recy- 2Max-Planck-Institute for Terrestrial Microbiology, Karl- cling of nutrients by the primary producers. This above- von-Frisch-Straße, 35043 Marburg, Germany. and below-ground feedback interaction constitutes the basis for ecological functioning of soil ecosystems (Wardle et al., 2004). The below-ground carbon flow has been Summary investigated in various soil–plant systems (Lynch and Root-derived carbon provides a major source for Whipps, 1990). However, little is known about the soil microbial production and emission of CH4 from rice microbiota that mediate the rhizosphere carbon dynamics. field soils. Therefore, we characterized the structure In carbon dynamics models (Paustian et al., 1997), the and activity of the bacterial community inhabiting rice below-ground biota, which consists of complex and roots and the rhizosphere. In the first experiment, diverse eukaryotic and prokaryotic life, is often considered DNA retrieved from rice roots was analysed for bac- as a ‘black box’. terial 16S rRNA genes using cloning, sequencing and In rice field soils, the below-ground carbon flow provides in situ hybridization. In the second experiment, rice an important carbon source for methane (CH4) production 13 plants were pulse-labelled with CO2 (99% of atom and emission. Early studies speculated that increasing 13C) for 7 days, and the bacterial RNA was isolated root exudation due to accelerated plant growth caused the from rhizosphere soil and subjected to density late season maxima of CH4 emission (Seiler et al., 1984; gradient centrifugation. RNA samples from density Schütz et al., 1989a). Isotope tracer experiments proved fractions were analysed by terminal restriction that the plant-photosynthesized carbon was rapidly (within fragment length polymorphism fingerprinting, cloning 3–5 h) allocated to the below-ground biosphere, trans- and sequencing. The experiments showed that the formed to CH4 and emitted into the atmosphere (Minoda dominant bacteria inhabiting rice roots and the and Kimura, 1994; Minoda et al., 1996; Dannenberg and rhizosphere particularly belonged to the Alphapro- Conrad, 1999). However, the microbiological mechanisms teobacteria, Betaproteobacteria and Firmicutes. The of root exudate decomposition and CH4 production RNA stable isotope probing revealed that the bacteria remained unclear. Owing to leakage of O2 and organic actively assimilating C derived from the pulse- substances from roots, the rice roots and the rhizosphere labelled rice plants were Azospirillum spp. (Alphapro- provide niches for diverse organisms performing various teobacteria) and members of Burkholderiaceae biogeochemical processes. The leakage of O2 supports (Betaproteobacteria). Both anaerobic (e.g. Clostridia) the oxidation of ammonia to nitrite, sulfide to sulfate, fer- and aerobic (e.g. Comamonas) degraders were rous iron to ferric iron, and CH4 to CO2. On the other hand, present at high abundance, indicating that root envi- denitrification, reduction of iron and sulfate and methano- ronments and degradation processes were highly het- genesis occur in the adjacent zone of anaerobic soil (Lie- erogeneous. The relative importance of iron and sack et al., 2000). Organic substances released from rice sulfate reducers suggested that cycling of iron and roots serve as an important carbon and energy source for sulfur is active in the rhizosphere. the microbial activities in the rhizosphere. Some of the organisms responsible for the turnover of C, N, S and Fe have been identified using either cultivation-dependent or Introduction cultivation-independent methods. For example, the meth- It is widely recognized that the above-ground and below- ane-oxidizing bacteria in the rice rhizosphere include both ground biosphere supports and codepends on each other. type I and type II methanotrophs (Bodelier et al., 2000; Eller and Frenzel, 2001; Horz et al., 2001), but rice plants Received 14 December, 2005; accepted 22 February, 2006. *For + correspondence. E-mail [email protected]; Tel. (+49) and NH4 fertilization apparently stimulate the activity of 6421 178 801; Fax (+49) 6421 178 809. the type I methanotrophs (Bodelier et al., 2000; Eller and © 2006 The Authors Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd 转载 中国科技论文在线 http://www.paper.edu.cn 1352 Y. Lu, D. Rosencrantz, W. Liesack and R. Conrad Frenzel, 2001). Nitrosomonas is considered the major Table 1. Phylogenetic affiliation and number of bacterial 16S rRNA ammonia oxidizer on rice roots (Nicolaisen et al., 2004). gene clones retrieved from rice roots at the age of 45 days and 90 days. The structure of nitrate-reducing bacteria on rice roots is unclear, but the addition of nitrate largely increased the Clone library Day 45 Day 90 growth of Bacillus and Dechloromonas (Scheid et al., Phylogenetic group 2004), which are capable of denitrification. Both Gram- Alphaproteobacteria positive Desulfosporosinus spp. and members of Desulfo- Bradyrhizobiaceae 1 bacteraceae and Desulfovibrionaceae are possibly Caulobacteraceae 1 Rhizobiaceae 2 responsible for sulfate reduction in the Italian rice soils Hyphomicrobiaceae 11 (Scheid and Stubner, 2001; Scheid et al., 2004). Geo- Rhodospirillaceae 1 bacter, Pelobacter and, interestingly, the Anaeromyxo- Sphingomonadaceae 4 Rickettsiaceae 4 bacter group seem to be involved in ferric iron reduction Betaproteobacteria in the rhizosphere (Treude et al., 2003; Scheid et al., Comamonadaceae 215 2004). Rhodocyclaceae 26 Hydrogenophilaceae 2 An analysis of carbon flow through the different com- Deltaproteobacteria partments of the rhizospheric microbiota is essential to Geobacteraceae 2 understand the microbe-driven C and nutrient cycling in Myxococcales 66 Gammaproteobacteria the rhizosphere. Phospholipid fatty acids-based stable Pseudomonadaceae 1 isotope probing (SIP) has been used to link the rhizo- Firmicutes spheric carbon flow to the microbial community (Butler Clostridium 87 Sporomusa 25 et al., 2003; Lu et al., 2004; Treonis et al., 2004). However, Cyanobacteria 1 phospholipid fatty acids-SIP can only provide a coarse Actinobacteria 11 resolution of the microbial phyla (Singh et al., 2004). Acidobacteria 52 Bacteroidetes 27 Recently, Rangel-Castro and colleagues (2005) applied 13 RNA-SIP to a CO2-pulse-labelled grassland community and found that only a few members of the highly diverse community of bacteria, archaea and fungi became specif- daceae and Rhodocyclaceae of the Betaproteobacteria ically labelled if the grassland had been limed. each accounted for approximately 5% of total clones. We have previously identified the key archaeal groups In the 90-day library, Comamonadaceae-like clone involved in CH4 production in the rice rhizosphere by sequences were most abundant, followed by those 13 applying RNA-SIP to a CO2-pulse-labelled archaeal assigned to Clostridia and Bacteroidetes. Myxococcales, community (Lu and Conrad, 2005). In the present study, Rhodocyclaceae, Sporomusa, Sphingomonadaceae and the bacterial community inhabiting rice roots and rhizo- Rickettsiaceae each accounted for 5–10% of total clones. sphere was determined by a combination of 16S rRNA The frequency of Deltaproteobacteria-like clone se- gene clone library analysis and rRNA-targeted fluores- quences relatively decreased while the clone frequency cence in situ hybridization (FISH). The active populations of Alpha- and Betaproteobacteria (20% and 36% of 64 were identified by RNA-SIP analysis using material from clones respectively) increased in the 90-day library as our previous pulse-labelling experiment (Lu and Conrad, compared with the 45-day library. The sequences related 2005). to Proteobacteria accounted for 44–66% of total clones sequenced in both clone libraries. Results Fluorescence in situ hybridization revealed that bacte- rial cells were distributed both on and inside the root Structure of bacterial community on rice roots tissues (Fig. 1A and B). Highly dense populations of Bac- (experiment I) teria were detected on root tips (Fig. 1C). Members of the Two clone libraries were constructed to characterize the Betaproteobacteria were the most abundant populations bacterial community inhabiting rice roots: one from 45- both on 27- and 85-day-old roots. Alphaproteobacteria, on day-old rice roots (34 clones) and the other from 90-day- the other hand, were barely detectable by FISH. old rice roots (64 clones). Comparative analyses of envi- ronmental 16S rRNA gene sequences showed that the Active bacteria associated with rhizosphere carbon flow root-associated bacterial community is phylogenetically (experiment II) diverse (Table
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