Elsevier

Science of The Total Environment

Volume 665, 15 May 2019, Pages 171-180
Science of The Total Environment

Anammox response to natural and anthropogenic impacts over the Yangtze River

https://doi.org/10.1016/j.scitotenv.2019.02.096Get rights and content

Highlights

  • Anammox bacterial abundance and alpha diversity increased towards the river mouth along a temperature gradient.

  • Anammox contribution to N2 production decreased towards the river mouth due to enhanced denitrification process

  • Dam-induced sediment coarsening decreased anammox bacterial diversity.

  • The Three Gorges Dam enhanced anammox role in nitrogen loss.

Abstract

Increasing attention has been paid to anaerobic ammonium oxidation (anammox) in river ecosystems due to their special role in the global nitrogen cycle from land to the ocean. This study have revealed the spatial patterns of anammox bacterial response to geographic characteristics and dam operation along the Yangtze River, using 15N tracers and molecular analyses of microbial communities in sediment samples over a 4300 km continuum. Here we found a significant temperature-related increase in anammox bacterial abundance and alpha diversity from mountainous area in the upper, fluvial plain area in the middle and lower reach, to the river mouth. In contrast, an opposite trend in anammox contribution to N2 production (ra) was observed down the Yangtze River due to enhanced denitrification induced by spatial heterogeneity of total organic carbon. Interestingly, the Three Gorges Dam resulted in an intensive erosion and thus a change from muddy to sandy sediments within 400 km downstream the dam, which readjusted the anammox community characterized with a decreased bacterial diversity and enhanced anammox contribution to nitrogen loss. Our study highlights the importance of natural and anthropogenic impacts on anammox bacterial community and function in a complex large river ecosystem.

Introduction

Rivers are the cradle of human civilization, such as the Yangtze River civilization and the Indus Valley civilization, and historical human settlements have followed river networks. Rivers link terrestrial and marine biospheres by transporting organic material and nutrients from the land to the ocean (Cole et al., 2007). Many large dams have been built to generate hydropower to meet the demand for rapid economic development downstream of large rivers. This remarkably alters the geomorphic, hydraulic, and sediment characteristics of large rivers (Baker et al., 2011; Csiki and Rhoads, 2010; Graf, 2006; Lai et al., 2017). On the contrary, the origin zones of large rivers are maintained in their original ecological attributes because they are far away from the center of human activity (Kang et al., 2002; Qiu, 2008). Hence, research regarding watersheds of huge river systems has made it possible to explore the effects of species evolution and geological change attributed to natural and anthropogenic impacts more clearly.

Microorganisms are ubiquitous in river ecosystems where they play key roles in biogeochemical processes such as nutrient transformation and energy flow (Madsen, 2011; Savio et al., 2015). In recent years, anaerobic ammonium oxidation (anammox) has received great attention owing to its crucial role and special pathway in the nitrogen cycle in freshwater ecosystems (Hoagland et al., 2019; Sonthiphand et al., 2014; Zhu et al., 2013; Zhu et al., 2015). Anammox occurrence has been found in aquatic ecosystems at different scales, including regional-scale estuarine wetland sediments (Dale et al., 2009) and paddy soils (Yang et al., 2015), local-scale river permeable sediments (Lansdown et al., 2016) and wetland lake sediments (Zhu et al., 2013), and micrometer-scale rhizosphere soils (Nie et al., 2015). However, there remains a lack of knowledge concerning their spatial patterns and its potential driving factors along basin-scale river networks.

Large rivers flow through various landform types, different soil hydraulic and physicochemical properties, and different intensities of human alteration. Discrepant landforms result in different climatic zones owing to their steepness of slope and elevation (Swanson et al., 1988), and affect the ways of delivery of resources to microbial active zones (Bissett et al., 2013; Mohammadi et al., 2017; Tatariw et al., 2013). Nevertheless, the roles of landform type or structure in determining anammox community structure, diversity, and activity are poorly known. Large rivers are often interrupted by human activities, most noticeably by artificial damming, which can significantly alter physicochemical and biological properties before and after the dam (Ruiz-González et al., 2013). Damming influences on bacterial community structure or functional gene (e.g., nitrogen, phosphorus, and sulfur cycling genes) diversity have been reported previously (Ruiz-González et al., 2013; Wu et al., 2015; Yan et al., 2015). Further, large dams can alter sediment types directly (Ligon et al., 1995; Phillips et al., 2005). Different sediment types shape the bacterial abundance and community structure, as these are influenced by permeability (Gobet et al., 2012; Schöttner et al., 2011), and anammox bacterial diversity can be determined by nutrient concentrations and sediment grain size in marine sediments (Bale et al., 2014; Dang et al., 2010). As such, we would expect a possible differentiation of anammox bacterial community or diversity before and after the dams. Herein, we hypothesized that anammox bacterial traits would occur widely in large rivers and show great heterogeneity. This heterogeneity would be shaped by geographical factors such as landform and change of sediment type induced by artificial damming and not just the previously reported substrate nutrients (Yang et al., 2015).

To address these hypotheses, we collected sediment samples from monitoring stations that ranged over a 4300 km continuum of Asia's largest river, the Yangtze River. The effects of river environmental factors (e.g., NH4+, NOx, TN) and damming (Three Gorges Dam (TGD), the world's largest dam), on anammox bacterial abundance, community structure, activity and their contribution to nitrogen production (ra) were statistically analyzed. Structural equation modeling (SEM) was used to evaluate the relative importance of various pathway regulate anammox activity and their contribution to N2 production. Meanwhile, the suitable niches of anammox bacteria along the Yangtze River were systematically illustrated from the aspects of temperature, sediment permeability, and sediment coarsening. This unprecedented investigation over a large-scale river network offers the geographical insight into anammox occurrence in a large river.

Section snippets

Study area and background

The Yangtze River is the largest river in Asia and the third longest river by discharge volume in the world. It flows for 6300 km from the glaciers on the Qinghai-Tibet Plateau in Qinghai eastward across southwest, traverses nine provinces from west to east, and finally pours into the East China Sea (Chen et al., 2001; Milliman and Meade, 1983). A total of 23 sampling sites on the main stream were chosen for the present study. Our sampling sites cover 4300 km Yangtze River from Shigu in the

Spatial distribution of anammox bacterial abundance and diversity

Positive PCR products were obtained for all sediment samples from the Yangtze River. The number of anammox hzsA genes ranged from 10^5 to 10^8 gene copies per gram of dry sediment (Fig. S1). In total, 412,736 sequences were obtained (Fig. S2) and >5 genera of anammox bacteria, Brocadia, Kuenenia, Jetternia, Scalindua, and Anammoxglobus were detected in the sediments along the Yangtze River with high diversity (Fig. S3 and Fig. S4).

The amount of anammox bacteria showed significant and negative

Temperature shaping anammox bacterial spatial patterns

This study has delineated anammox bacterial spatial patterns and responses to anthropogenic activities (damming) over a 4300 km longitudinal transect of the Yangtze River. It should be noted that our study underlines large-scale geographical factors shaping anammox bacteria, which is contrary to previous studies that have researched substrate nutrient effects only (Lansdown et al., 2016; Nie et al., 2015; Wang et al., 2017). The present study has undoubtedly improved our understanding of

Conclusion

In summary, the present study has investigated the integrated influence of natural and anthropogenic impacts on the spatial patterns of anammox bacterial traits along the Yangtze River. Anammox bacterial abundance and alpha diversity increased significantly towards the river mouth along a temperature gradient. Further, anammox activity and ra showed significant spatial patterns along the river, and SEM results revealed that TOC and anammox bacterial alpha diversity directly shaping the spatial

Conflict of interest

The authors declare no competing financial interests.

Acknowledgements

Financial support from Fund for Innovative Research Group of NSFC (Grant No. 51721006) should also be highly appreciated.

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