Distinct strategies of abundant and rare bacterioplankton in river-reservoir system: Evidence from a 2800 km plateau river

https://doi.org/10.1016/j.envres.2021.111418Get rights and content

Highlights

  • 16S rRNA gene sequencing and Geochip microarray data sets were matched.

  • Total taxonomy and functional traits were determined by different sub-communities.

  • Abundant sub-community exhibited functional redundancy in response to damming.

  • Rare sub-community maintained a greater stability due to portfolio effect.

  • Dispersal process of the dominated sub-community was less susceptible to damming.

Abstract

Riverine bacterioplankton are highly responsive to river alterations and their abundant and rare sub-communities may have different roles in biogeochemical cycling. However, with the rapid development of dam constructions, our knowledge on adaptation mechanism of these sub-communities in regulated river ecosystem was still limited, especially with regard to their functional traits. Here, our study was conducted in the 2800 km Yarlung Tsangpo River on the Tibetan Plateau to address the question of how abundant and rare bacterioplankton would respond taxonomically and functionally to river damming using 16S rRNA gene sequencing combined with Geochip microarray technique. Our results showed that abundant sub-community dominated taxonomic composition while rare sub-community largely determined functional composition. It is also observed that taxonomic diversity of abundant sub-community was significantly stimulated in the reservoir while that of rare sub-community was markedly inhibited. Moreover, abundant sub-community exhibited functional redundancy under damming disturbances since altered taxonomic composition and unaltered functional composition co-occurred simultaneously. Meanwhile, due to portfolio effect, rare sub-community maintained a greater stability under damming disturbances with little variation in taxonomic and functional compositions. In addition, the Stegen null model analysis revealed that stochastic process governed community assembly in both abundant and rare sub-communities. However, according to source tracking analysis, the taxonomic dispersion of abundant sub-community was less significantly impeded by the dam while the functional dispersion of rare sub-community was less strongly interrupted, indicating that the dispersal process in the dominated sub-community was less susceptible to damming. Therefore, by considering bacterioplankton functional traits, our study provided comprehensive evidences for the distinct strategies of abundant and rare sub-communities in response to damming.

Introduction

Rivers transport water, sediment and nutrients from terrestrial to marine ecosystems and participate in important regional and global biogeochemical cycles (Grill et al., 2019). However, due to social and economic development in recent decades, many rivers worldwide are now suffering from anthropogenic disturbances, such as damming (Tonkin et al., 2019). It is widely suggested by previous studies that the construction of dams may result in significant impacts on ecosystem functions and services (Akbarzadeh et al., 2019; Maavara et al., 2020). Being an essential component in aquatic ecosystems, bacterioplankton are major drivers of biogeochemical cycling and river ecosystem productivity (Xia et al., 2017; Kuypers et al., 2018; Zhang et al., 2020). Compared with macroscopic communities, bacterioplankton communities are much more diverse and are highly responsive under environmental perturbations due to their rapid growth rate (Hassell et al., 2018). Since dams may influence ecosystem function by altering bacterioplankton communities (Ruiz-González et al., 2013; X. Wang et al., 2018), a quantitative understanding of bacterioplankton communities is essential for estimating damming disturbances on river ecosystems. Yet the knowledge of biogeographic patterns of bacterioplankton in dammed rivers is still scarce over broad scales.

It is commonly recognized that bacterioplankton communities are highly diverse and unevenly distributed: a small number of high-abundance species (known as “abundant biosphere”) co-occur with a large number of low-abundance species (known as “rare biosphere”) (Jia et al., 2018; Lynch and Neufeld, 2015). Traditionally, despite of their small proportion of the entire community, studies has been focused on abundant bacterioplankton species because they are thought to be the most distributed and important in biogeochemical cycling (Chen et al., 2020; Niño-García et al., 2016; Read et al., 2015). However, recent studies have paid increasing attention on ecological importance of rare species since they can serve as a back-up taxa pool to contribute to the overall community stability by rapidly responding to environmental changes (Shade et al., 2014). Jiao et al. reported different biogeography distribution patterns for abundant and rare species under environmental disturbance (Jiao et al., 2017), while Liao et al. observed similar distribution of abundant and rare taxa in 21 lakes on Yungui Plateau in China (Liao et al., 2017). Hence, it remains unclear whether abundant and rare taxa exhibit similar distribution pattern in terms of taxonomic composition. Moreover, the bacterioplankton ecological stability is composed of not only taxonomic composition, but also functional traits (Anderson et al., 2011; Findlay, 2010). However, compared with taxonomic composition, few studies of functional traits was reported due to difficulties in distinguishing abundant and rare functions in bacterioplankton communities (Jia et al., 2018). Fortunately, Liang et al. recently proposed that rare taxa sub-community might be functionally more diverse than abundant taxa sub-community in terms of microbial nitrogen transformation (Liang et al., 2020). Since taxonomy together with functional traits constitute the active bacterioplankton community, it is essential to reveal the biogeographic pattern of taxonomic and functional composition simultaneously for maintaining ecological functions in river ecosystems.

With the dramatically rapid development of high throughput DNA sequencing technologies, we are now able to characterize the distribution of bacterioplankton communities at multiple levels of resolution (Graham et al., 2016). But it still remains challenging to advance beyond the question of “who is there?” and “what are they capable of doing?” to a more comprehensive understanding of the mechanisms structuring bacterioplankton communities (Grossart et al., 2020). The microbial communities can be assembled by either deterministic (environmental selection-related) process or stochastic (dispersal-related) process (Stegen et al., 2013; Zhou and Ning, 2017). But limited studies have investigated the assembly mechanisms of abundant and rare taxa sub-communities, and no agreement has been achieved. Chen et al. reported that environmental selection process influenced the abundant bacterioplankton sub-community more strongly than the rare sub-community in the upper Yangtze River (Chen et al., 2020), while the abundant and rare microbial sub-communities were both governed by stochastic process in the Tingjiang River (W. Chen et al., 2019b). Besides, it is also proposed that instead of being determined by a single process, the rare bacterioplankton assemblages might be shaped by more than one ecological processes in the subtropical bays (Mo et al., 2018). Therefore, the urgency of exploring the assembly mechanisms of abundant and rare sub-communities has never been greater as it can elucidate river ecosystem stability and multifunctionality mediated by bacterioplankton (Jousset et al., 2017).

The Yarlung Tsangpo River originates from the Tibetan Plateau and is known as the “Water Tower of Asia” due to its abundant hydropower resources (Sang et al., 2016). Extending over 2800 km and being the greatest plateau river in China, the hydropower development of the Yarlung Tsangpo River will vigorously solve the energy shortage and promote the sustainable development of regional economy in China (Winemiller et al., 2016). The first and currently the only dam in its main stream is the Zangmu Dam which began to operate in late 2015. Meanwhile, as located in plateau regions, the river ecosystem in the Yarlung Tsangpo River is much more vulnerable than in plain regions (Frindte et al., 2019), which might be more susceptible to river damming.

In our study, the combination of 16S rRNA gene sequencing and metagenomic tool of Geochip was conducted to explore the taxonomic and functional variations in abundant and rare bacterioplankton along the dammed Yarlung Tsangpo River. We hypothesize that abundant and rare sub-communities would exhibit distinct taxonomic and functional patterns in response to river damming. Therefore, the main aims of our study are to: i) investigate whether the taxonomic and functional distributions of different bacterioplankton sub-communities would respond equally to river damming; ii) unravel the taxonomic and functional assembly mechanisms of abundant and rare sub-communities under damming disturbances.

Section snippets

Study area and sample collection

As one of the highest river in the world, the average elevation of the Yarlung Tsangpo River is over 4200 m (Jiang et al., 2015). The height of the Zangmu Dam is 116 m with a total reservoir storage of 8.7 × 107 m3. The installed capacity of the Zangmu power station is 510 MWh and it began in operation in late 2015 (P. Wang et al., 2017). The field sampling of the Yarlung Tsangpo River was conducted from April to May 2017, including 35 sampling sites and covering more than 2100 km (Fig. 1). The

Distribution of α-diversity in bacterioplankton community at different levels

The total qualified sequences ranged from 28435 to 51379 in the 105 bacterioplankton samples in the Yarlung Tsangpo River. A total of 12496 annotated OTUs were detected in the total bacterioplankton community, while 0.61% (76) and 84.87% (10605) of the OTUs were presented in the abundant and rare sub-communities (Table S3). However, in contrary to OTU number, the relative abundance of rare taxa (2.02%) was significantly lower than that of abundant taxa (78.74%), suggesting that abundant

Different biogeographic patterns between abundant and rare sub-communities in the dammed Yarlung Tsangpo River

In our study, rare OTUs have lower abundance but extremely higher number when compared to abundant OTUs, and rare sub-community exhibited significantly higher α-diversity. These findings suggested that although rare taxa are not dominant in total taxonomic community, they may still play important roles in maintaining the overall community stability due to their large taxa pool (Galand et al., 2009; Liang et al., 2020). Thus, it has been reported that rare taxa serve as an insurance source of

Conclusion

Our results showed that abundant taxa sub-community dominated the total taxonomic composition while rare taxa sub-community largely determined the total functional composition. River damming significantly stimulated the taxonomic diversity of abundant taxa while that of rare taxa was markedly inhibited. Moreover, abundant sub-community exhibited functional redundancy under damming disturbances since altered taxonomic composition and unaltered functional composition co-occurred simultaneously.

Data accessibility

The bacterioplankton DNA sequencing data have been submitted to the Sequence Read Archive (SRA) of the National Center for Biotechnology Information (NCBI) database under Accession No. SRP167709.

Author contributions

Xun Wang: Conceptualization, Methodology, Software, Investigation, Writing – Original Draft, Visualization. Peifang Wang: Conceptualization, Writing – Review & Editing. Chao Wang: Conceptualization, Writing – Review & Editing. Juan Chen: Investigation, Resources. Bin Hu: Investigation, Resources. Sheng Liu: Investigation, Resources. Qiusheng Yuan: Investigation, Resources.

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

We wish to thank Dr. Tao Feng from Fisheries and Oceans Canada, Bedford Institute of Oceanography for his assistance in creating the sampling map. This work was supported by the Key Program of National Natural Science Foundation of China (92047201), the National Science Funds for Creative Research Groups of China (51421006), the National Key Plan for Research and Development of China (2016YFC0502203), the National Natural Science Foundation of China (42007149), Key Program of National Natural

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