Nitrogen cycling processes and the role of multi-trophic microbiota in dam-induced river-reservoir systems

Highlights

• Dams affect nitrogen (N) cycling in river-reservoir systems.

• N cycling processes vary along the longitudinal and the vertical gradient.

• Multi-trophic microbiota participate in N cycling in direct and indirect ways.

• Ecological studies should consider multi-trophic levels and their interactions.

Abstract

The nitrogen (N) cycle is one of the most important nutrient cycles in river systems, and it plays an important role in maintaining biogeochemical balance and global climate stability. One of the main ways that humans have altered riverine ecosystems is through the construction of hydropower dams, which have major effects on biogeochemical cycles. Most previous studies examining the effects of damming on N cycling have focused on the whole budget or flux along rivers, and the role of river as N sources or sinks at the global or catchment scale. However, so far there is still lack of comprehensive and systematic summarize on N cycling and the controlling mechanisms in reservoirs affected by dam impoundment. In this review, we firstly summarize N cycling processes along the longitudinal riverine-transition-lacustrine gradient and the vertically stratified epilimnion-thermocline-hypolimnion gradient. Specifically, we highlight the direct and indirect roles of multi-trophic microbiota and their interactions in N cycling and discuss the main factors controlling these biotic processes. In addition, future research directions and challenges in incorporating multi-trophic levels in bioassessment, environmental flow design, as well as reservoir regulation and restoration are summarized. This review will aid future studies of N fluxes along dammed rivers and provide an essential reference for reservoir management to meet ecological needs.

Introduction

Rivers are important channels connecting terrestrial and marine ecosystems and serve as transportation systems for large amounts of materials and nutrients. Currently, more than 50% of global rivers are fragmented by dams for hydropower production, water supply, flood control, and navigation (Grill et al., 2019). Dam construction has major effects on hydro-geomorphology, biogeochemical cycles, and the ecological environment. First, dams convert rivers into lentic reservoirs characterized by decreased flow velocity and increased hydraulic residence time (Nilsson et al., 2005). Hydrological variations associated with damming also affect annual runoff, thermal regimes, and sediment loads (Wang et al., 2016; Yigzaw et al., 2019). Second, dams disrupt the river continuum, which increases nutrient loads and induces changes in nutrient stoichiometric ratios along river systems (Wang et al., 2018a). Third, hydrological and biogeochemical variations reshape riparian and riverine habitats and alter the structure, diversity, and distribution of biological communities (Poff et al., 2007). Ultimately, dams can modify the ecosystem functions (e.g., nutrient cycling and energy flow) and services (e.g., fisheries) of rivers (Turgeon et al., 2019).

Nutrients such as carbon (C), nitrogen (N), phosphorus (P), and silicon (Si) are transported along rivers. Damming can alter riverine nutrient cycles in multiple and complex ways and have positive or negative impacts. For example, reservoirs can eliminate nutrients from the water column via sedimentation or gaseous release, thus alleviating eutrophication pressure on downstream ecosystems (Van Cappellen and Maavara, 2016). However, the longer hydraulic residence time and the higher transparency may promote primary productivity and nutrient transformation within reservoirs, resulting in increased eutrophication downstream (Chen et al., 2018). Reservoirs tend to facilitate the retention of nutrients from rivers in large quantities. Taylor Maavara from the University of Waterloo has quantified the effects of dams on C, P, Si, and N fluxes based on global data. They estimated that the global primary productivity and C mineralization ratio (P/R) will double by 2030 because of damming (Maavara et al., 2017). Meanwhile, approximately 17% and 5.3% of the global total P and total reactive Si loading to rivers are expected to be sequestered in reservoirs, respectively (Maavara et al., 2014, 2015). Compared with P and Si, which are eliminated most efficiently in reservoirs through particle sedimentation, N cycling within reservoirs is more complex and is typically dominated by transformation processes. Reservoirs contributed approximately 33% of the total N removed by lentic systems in 2000, and denitrification and burial eliminated 7% of N loading to the global river network; this is predicted to double to 14% by 2030 (Akbarzadeh et al., 2019; Harrison et al., 2009). Recently, a review article by Maavara et al. (2020) discussed the impacts of damming on the biogeochemistry of these nutrients along river networks from a global perspective. The authors emphasized that responsible dam construction and management require consideration of nutrient elimination and loading to achieve a balance between environmental impacts and damming services.

Given the relative complexity of N transformation, a complete knowledge of N cycling processes in reservoirs and dammed river systems is critically important. N inputs to reservoirs are transformed by a series of biotic and abiotic processes, such as nitrification and denitrification, biological assimilatory uptake, sedimentation, and benthic release (Keys et al., 2019; Ran et al., 2017). The cycle of N in river systems was reviewed by Xia et al. (2018), summarizing a series of N transformation pathways active in the water column, suspended particle-water surfaces in overlying water, sediment-water interfaces, and riparian zones. N transformations in rivers and streams are mainly controlled by microbial-mediated oxidation and reduction processes and thus are usually referred to as the microbial N cycle. Several researchers have summarized these biological processes (Kuypers et al., 2018; Zhang et al., 2020b). Briefly, dinitrogen gas (N₂) is first fixed to ammonia N (NH₄⁺), which is assimilated into organic N. The degradation of organic N through ammonification can in turn release NH₄⁺, which is subsequently oxidized to nitrite (NO₂⁻) and nitrate (NO₃⁻) through the nitrification process and eventually converted back to N₂ via denitrification and anammox processes. The N cycling in river systems is influenced by both natural and man-made disturbances. Rivers are being changed because of human activities, and damming is the most severe anthropogenic disturbance. The widespread construction of dams and reservoirs may impede the hydrologic connectivity of rivers, limit physical exchange, modify the distribution of species, and result in variation in N transformation and flux (Akbarzadeh et al., 2019; Gao et al., 2021b).

The importance of N as a biogenic element and water quality indicator has motivated several studies of N cycling in river systems. As mentioned above, some related review articles have summarized the processes, mechanisms, and drivers of N cycling, as well as the methods for identifying the sources of N or tracing the flux of N (Xia et al., 2018; Zhang et al., 2020b). Dam construction has long been a major focus of research. Published review articles have mainly focused on the entire N budget or flux along rivers and the role of rivers as N sources or sinks affected by damming at the global or catchment scale (Akbarzadeh et al., 2019; Maavara et al., 2020; Van Cappellen and Maavara, 2016; Wang et al., 2018a). However, no studies to date have comprehensively characterized N cycling processes and the controlling factors within a relatively small region, i.e. river-reservoir systems. This review provides a comprehensive overview of N cycling processes along both the longitudinal river flow gradient and the vertical water column gradient for the first time. We summarize the role of multi-trophic microbiota and their biotic and abiotic interactions, which have often been overlooked by previous studies, in controlling N cycling in river-reservoir systems. Learning and mastering these N cycling processes in a single reservoir is key for understanding N patterns along entire rivers. The goal of this review is to promote future research on N cycles along dammed rivers, as well as provide guidance for the restoration of trophic conditions and management of reservoirs from an ecosystem perspective.