Elsevier

Applied Soil Ecology

Volume 157, January 2021, 103762
Applied Soil Ecology

Metabolic potential and community structure of bacteria in an organic tea plantation

https://doi.org/10.1016/j.apsoil.2020.103762Get rights and content

Highlights

  • Soil-associated community showed higher metabolic potential and diversity.

  • Bacterial families with niche preferences in different rhizo-compartments were demonstrated.

  • Organic tea plantations provide opportunities to study uncultivated bacteria.

Abstract

Revealing the spatial and temporal distribution of bacteria in organic tea plantations is of great importance to clarify soil- and/or tea plant-associated community. In this study samples were collected from three rhizo-compartments of tea plant during four seasons, which were further subjected to community level physiological profiling and 16S rDNA next generation sequencing. Organic fertilization caused a short-term disturbance on pH, EC, and organic matter content of soil. Three rhizo-compartments harbored distinct bacterial community as revealed by PCA, PCoA and UPGMA analysis. Utilization of six carbon source categories was positively correlated with root surface community while negatively correlated with root interior community. Although there were variations in microbial parameters during four seasons, higher metabolic potential and diversity were observed in soil-associated rhizo-compartments. Bacterial families Gemmataceae, Pedosphaeraceae, and Solibacteraceae were more abundant in soil and root surface, while root interior were dominated by families Acidothermaceae, Burkholderiaceae, Ktedonobacteraceae, and Xanthobacteraceae. It is proposed that Burkholderiaceae and Xanthobacteraceae which dominate in root surface or root interior samples and other poorly studied phylogenetic groups may serve as potential candidates to study their interaction with tea plant.

Introduction

Roots provide different microhabitats at the soil-root interface, which include rhizosphere soil, rhizoplane, and endorhizosphere where the complex plant-microbe interactions occurred (Reinhold-Hurek et al., 2015). Experimental evidences have underlined the importance of the root microbiome in plant health and it is becoming increasingly clear that the plant is able to control the composition of its microbiome (Berendsen et al., 2012). It was demonstrated that microbial communities derived from roots or rhizosphere were significantly different from that in bulk soil (Gkarmiri et al., 2017). Within soil ecosystems, pH plays a crucial role in determining bacterial communities and showed potential as the best predictor of bacterial community composition (Lauber et al., 2008; Rousk et al., 2010; Kim et al., 2014; Long et al., 2015). The acidic nature of red soil commonly found in tea plantation may provide unique habitats for the growth of various bacterial groups (Lynn et al., 2017). However, there are only few studies dealt with bacterial community associated with tea plants (Camellia sinensis).

Goswami et al. (2017) obtained 70 acid-tolerant isolates from tea plantation and showed that low soil pH influenced bacterial community structure and their functional properties. Using pyrosequencing Li et al. (2016) indicated that Gammaproteobacteria, Alphaproteobacteria, Acidobacteria, and Actinobacteria were the main phyla in the tea orchard soils. Lynn et al. (2017) also demonstrated that tea plantation was rich in Actinobacteria, followed by Chloroflexi, Acidobacteria, Proteobacteria, and Firmicutes. Other dominant phyla found in tea plantation included Cyanobacteria, Bacteroides, Nitrospirae, Verrucomicobia, and Gemmatimonadetes (Arafat et al., 2017). The relative abundances of Chloroflexi and Acidobacteria increased continuously with the increasing age of tea plantations (Wang et al., 2019). Being an important economic crop worldwide, tea attracts much attention in its cultivation and manufacture techniques. In Taiwan, there are 12,079 ha of tea plantation, producing 14,738 tons per year (Council of Agriculture, 2018). Currently a total of 415 ha of tea plantation were cultivated organically (Council of Agriculture, 2019).

A key goal of rhizosphere microbial ecology is to facilitate the development of agricultural systems that deliver high levels of food security while reducing the environmental impacts (Dennis et al., 2010). Long-term fertilization with manure has been shown to increase the 16S rRNA gene copy numbers and bacterial diversity in both rhizosphere and bulk soil (Wang et al., 2018). Application of organic fertilizers increased the pH of acidic soil and also significantly increased organic carbon and nutrient contents, which contributed to higher root length and plant biomass (Zhang et al., 2019). Previously we also demonstrated that soils under long-term organic farming harbored diverse functional potential and metabolic activity of fast-growing heterotrophs, which may serve as valuable sites for microbial ecological study (Chou et al., 2017).

Next generation sequencing (NGS) technologies which target conserved regions of phylogenetic markers to obtain operational taxonomic units (OTUs) enhanced the study of complex microbial communities (Almeida and De Martinis, 2019). Clarification of bacterial community associated with root system helps in understanding the interactions between bacteria and their host, and also facilitates the development of more effective soil management strategies to sustain plant growth and health. In the present study samples were collected from soil, root surface and root interior of tea plants during four seasons, in order to test the hypothesis that different rhizo-compartments within organic tea plantations harbor different bacterial communities. These samples were further subjected to community level physiological profiling (CLPP) and 16S rDNA NGS to investigate the spatial and temporal distribution of bacteria and explore soil- and/or tea plant-associated community.

Section snippets

Site descriptions and sampling

Samples were collected from an organic tea plantation which is managed by the Tea Research and Extension Station and located in Yuchin, Nantou County, Taiwan (23°52′47″N, 120°54′46″E). Tea plant grown on this field is large-leaf cultivar TTES No. 8 (a variety transformed from the original Indian Assam tea plant), with the age almost 30 years old. Organic farming manipulation has been conducted here for almost 20 years, with the application of vegetative meals annually. During the research

Soil chemical property

The pH, EC, and organic matter content of tea plantation soils collected during four seasons were determined. After organic amendment notable changes in soil properties were observed between autumn and winter sampling period (Table 1). Application of organic fertilizer (sesame meal) led to the decrease of soil pH, which returned to similar level in samples collected in summer. Both EC and organic matter content of soil significantly increased in winter, and they also returned to similar value

Discussion

In view of spatial and temporal variations in bacterial community within tea plantation, samples derived from three rhizo-compartments were collected during four seasons to explore soil- and/or tea plant-associated community. Although there were variations in microbial parameters during four seasons, higher metabolic potential and diversity were observed in soil-associated community. The entire bacterial community or dominant families within root interior which formed less complex network were

Conclusions

In the present study bacterial communities derived from three rhizo-compartments in an organic tea plantation were well clarified. Both functional and population diversity were higher in soil-associated community when compared with that of root interior community. Higher metabolic activities recorded in soil and root surface samples might be related to the presence of dominant families such as Gemmataceae, Pedosphaeraceae, and Solibacteraceae. A distinct community dominated by Acidothermaceae,

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research work was kindly supported by grants from the Ministry of Science and Technology, Taiwan and in part by the Ministry of Education, Taiwan, R.O.C. under the Higher Education Sprout Project.

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